Molecular Basis of Fibrin Clot Elasticity

Structure

Volumn 16, Issue 3, 2008, Pages 449-459

  Lim, Bernard B C ^a   Lee, Eric H ^b   Sotomayor, Marcos ^c   Schulten, Klaus ^b,c  

^a Mayo Clinic   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c University of Illinois at Urbana Champaign   (United States)

Author keywords

CELLBIO; PROTEINS

Indexed keywords

CALCIUM ION; FIBRIN; FIBRINOGEN;

ALPHA HELIX; ARTICLE; ATOMIC FORCE MICROSCOPY; ELASTICITY; FIBRIN CLOT; MECHANICAL STRESS; PH; PRIORITY JOURNAL;

BLOOD COAGULATION; CALCIUM; COMPUTER SIMULATION; ELASTICITY; FIBRIN; FIBRINOGEN; HUMANS; HYDROGEN-ION CONCENTRATION; MICROSCOPY, ATOMIC FORCE; MODELS, BIOLOGICAL; MODELS, MOLECULAR; POLYMERS; PROTEIN STRUCTURE, SECONDARY;

EID: 40049099583     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2007.12.019     Document Type: Article

References (65)

1. Bornschlogl T., and Rief M. Single molecule unzipping of coiled coils: sequence resolved stability profiles. Phys. Rev. Lett. 96 (2006) 118102
2. Brown J.H., Volkmann N., Jun G., Henschen-Edman A.H., and Cohen C. The crystal structure of modified bovine fibrinogen. Proc. Natl. Acad. Sci. USA 97 (2000) 85-90
3. Brown A.E., Litvinov R.I., Discher D.E., and Weisel J.W. Forced unfolding of coiled-coils in fibrinogen by single-molecule AFM. Biophys. J. 92 (2007) L39-L41
4. Buck M., Bouguet-Bonnet S., Pastor R.W., and MacKerell Jr. A.D. Importance of the CMAP correction to the CHARMM22 protein force field: dynamics of hen lysozyme. Biophys. J. 90 (2006) L36-L38
5. Budzynski A.Z. Fibrinogen and fibrin: biochemistry and pathophysiology. Crit. Rev. Oncol. Hematol. 6 (1986) 97-146
6. Bullough P.A., Hughson F.M., Skehel J.J., and Wiley D.C. Structure of influenza haemagglutinin at the pH of membrane fusion. Nature 371 (1994) 37-43
7. Burkhard P., Stetefeld J., and Strelkov S.V. Coiled coils: a highly versatile protein folding motif. Trends Cell Biol. 11 (2001) 82-88
8. Cluzel P., Lebrun A., Heller C., Lavery R., Viovy J.L., Chatenay D., and Caron F. DNA: an extensible molecule. Science 271 (1996) 792-794
9. Collet J.P., Shuman H., Ledger R.E., Lee S., and Weisel J.W. The elasticity of an individual fibrin fiber in a clot. Proc. Natl. Acad. Sci. USA 102 (2005) 9133-9137
10. Doolittle R.F. Fibrinogen and fibrin. Annu. Rev. Biochem. 53 (1984) 195-229
11. Evans E., and Ritchie K. Dynamic strength of molecular adhesion bonds. Biophys. J. 72 (1997) 1541-1555
12. Everse S.J., Spraggon G., Veerapandian L., Riley M., and Doolittle R.F. Crystal structure of fragment double-D from human fibrin with two different bound ligands. Biochemistry 37 (1998) 8637-8642
13. Fowler W.E., Hantgan R.R., Hermans J., and Erickson H.P. Structure of the fibrin protofibril. Proc. Natl. Acad. Sci. USA 78 (1981) 4872-4876
14. Galanakis D.K. Fibrinogen anomalies and disease. A clinical update. Hematol. Oncol. Clin. North Am. 6 (1992) 1171-1187
15. Galanakis D.K. Inherited dysfibrinogenemia: emerging abnormal structure associations with pathologic and nonpathologic dysfunctions. Semin. Thromb. Hemost. 19 (1993) 386-395
16. Gao M., Craig D., Lequin O., Campbell I.D., Vogel V., and Schulten K. Structure and functional significance of mechanically unfolded fibronectin type III1 intermediates. Proc. Natl. Acad. Sci. USA 100 (2003) 14784-14789
17. Hall C.E., and Slayter H.S. The fibrinogen molecule: its size, shape, and mode of polymerization. J. Biophys. Biochem. Cytol. 5 (1959) 11-16
18. Humphrey W., Dalke A., and Schulten K. VMD: visual molecular dynamics. J. Mol. Graph. 14 (1996) 33-38 27-28
19. Isralewitz B., Gao M., and Schulten K. Steered molecular dynamics and mechanical functions of proteins. Curr. Opin. Struct. Biol. 11 (2001) 224-230
20. Izrailev S., Stepaniants S., Balsera M., Oono Y., and Schulten K. Molecular dynamics study of unbinding of the avidin-biotin complex. Biophys. J. 72 (1997) 1568-1581
21. Jorgensen W.L., Chandrasekhar J., Madura J.D., Impey R.W., and Klein M.L. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79 (1983) 926-935
22. Jung S.Y., Lim S.M., Albertorio F., Kim G., Gurau M.C., Yang R.D., Holden M.A., and Cremer P.S. The Vroman effect: a molecular level description of fibrinogen displacement. J. Am. Chem. Soc. 125 (2003) 12782-12786
23. Kiss B., Karsai A., and Kellermayer M.S. Nanomechanical properties of desmin intermediate filaments. J. Struct. Biol. 155 (2006) 327-339
24. Kohn W.D., Kay C.M., and Hodges R.S. Protein destabilization by electrostatic repulsions in the two-stranded α-helical coiled-coil/leucine zipper. Protein Sci. 4 (1995) 237-250
25. Kohn W.D., Monera O.D., Kay C.M., and Hodges R.S. The effects of interhelical electrostatic repulsions between glutamic acid residues in controlling the dimerization and stability of two-stranded α-helical coiled-coils. J. Biol. Chem. 270 (1995) 25495-25506
26. Kostelansky M.S., Betts L., Gorkun O.V., and Lord S.T. 2.8 A crystal structures of recombinant fibrinogen fragment D with and without two peptide ligands: GHRP binding to the "b" site disrupts its nearby calcium-binding site. Biochemistry 41 (2002) 12124-12132
27. Kumar S., Huang C., Zheng G., Bohm E., Bhatele A., Phillips J., Yu H., and Kale L. Scalable molecular dynamics with NAMD on Blue Gene. IBM J. Res. Dev. 52 (2007) 177-188
28. Li H., Linke W.A., Oberhauser A.F., Carrion-Vazquez M., Kerkvliet J.G., Lu H., Marszalek P.E., and Fernandez J.M. Reverse engineering of the giant muscle protein titin. Nature 418 (2002) 998-1002
29. Lim B.C. Atomic force microscopy of fibrinogen on different surface materials: implications for implantation. J. Thromb. Haemost. 88 (2005) 557
30. Lim B.C., Ariens R.A., Carter A.M., Weisel J.W., and Grant P.J. Genetic regulation of fibrin structure and function: complex gene-environment interactions may modulate vascular risk. Lancet 361 (2003) 1424-1431
31. Litvinov R.I., Gorkun O.V., Owen S.F., Shuman H., and Weisel J.W. Polymerization of fibrin: specificity, strength, and stability of knob-hole interactions studied at the single-molecule level. Blood 106 (2005) 2944-2951
32. Liu W., Jawerth L.M., Sparks E.A., Falvo M.R., Hantgan R.R., Superfine R., Lord S.T., and Guthold M. Fibrin fibers have extraordinary extensibility and elasticity. Science 313 (2006) 634
33. Lorand L. Factor XIII: structure, activation, and interactions with fibrinogen and fibrin. Ann. N Y Acad. Sci. 936 (2001) 291-311
34. Lorand L., Parameswaran K.N., and Murthy S.N. A double-headed Gly-Pro-Arg-Pro ligand mimics the functions of the E domain of fibrin for promoting the end-to-end crosslinking of gamma chains by Factor XIIIa. Proc. Natl. Acad. Sci. USA 95 (1998) 537-541
35. Lu H., Isralewitz B., Krammer A., Vogel V., and Schulten K. Unfolding of titin immunoglobulin domains by steered molecular dynamics simulation. Biophys. J. 75 (1998) 662-671
36. MacKerell Jr. A.D., Bashford D., Bellott M., Dunbrack Jr. R.L., Evanseck J.D., Field M.J., Fischer S., Gao J., Guo H., Ha S., et al. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B 102 (1998) 3586-3616
37. Mackerell Jr. A.D., Feig M., and Brooks III C.L. Extending the treatment of backbone energetics in protein force fields: limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations. J. Comput. Chem. 25 (2004) 1400-1415
38. Madrazo J., Brown J.H., Litvinovich S., Dominguez R., Yakovlev S., Medved L., and Cohen C. Crystal structure of the central region of bovine fibrinogen (E5 fragment) at 1.4-A resolution. Proc. Natl. Acad. Sci. USA 98 (2001) 11967-11972
39. Marchant R.E., Barb M.D., Shainoff J.R., Eppell S.J., Wilson D.L., and Siedlecki C.A. Three dimensional structure of human fibrinogen under aqueous conditions visualized by atomic force microscopy. Thromb. Haemost. 77 (1997) 1048-1051
40. Marszalek P.E., Lu H., Li H., Carrion-Vazquez M., Oberhauser A.F., Schulten K., and Fernandez J.M. Mechanical unfolding intermediates in titin modules. Nature 402 (1999) 100-103
41. Medved L., Ugarova T., Veklich Y., Lukinova N., and Weisel J. Electron microscope investigation of the early stages of fibrin assembly. Twisted protofibrils and fibers. J. Mol. Biol. 216 (1990) 503-509
42. Medved L., Tsurupa G., and Yakovlev S. Conformational changes upon conversion of fibrinogen into fibrin. The mechanisms of exposure of cryptic sites. Ann. N Y Acad. Sci. 936 (2001) 185-204
43. Nagar B., Overduin M., Ikura M., and Rini J.M. Structural basis of calcium-induced E-cadherin rigidification and dimerization. Nature 380 (1996) 360-364
44. Oberhauser A.F., Marszalek P.E., Erickson H.P., and Fernandez J.M. The molecular elasticity of the extracellular matrix protein tenascin. Nature 393 (1998) 181-185
45. Oesterhelt F., Oesterhelt D., Pfeiffer M., Engel A., Gaub H.E., and Muller D.J. Unfolding pathways of individual bacteriorhodopsins. Science 288 (2000) 143-146
46. Ortiz V., Nielsen S.O., Klein M.L., and Discher D.E. Unfolding a linker between helical repeats. J. Mol. Biol. 349 (2005) 638-647
47. Phillips J.C., Braun R., Wang W., Gumbart J., Tajkhorshid E., Villa E., Chipot C., Skeel R.D., Kale L., and Schulten K. Scalable molecular dynamics with NAMD. J. Comput. Chem. 26 (2005) 1781-1802
48. Pokutta S., Herrenknecht K., Kemler R., and Engel J. Conformational changes of the recombinant extracellular domain of E-cadherin upon calcium binding. Eur. J. Biochem. 223 (1994) 1019-1026
49. Rief M., and Grubmuller H. Force spectroscopy of single biomolecules. ChemPhysChem 3 (2002) 255-261
50. Rief M., Gautel M., Oesterhelt F., Fernandez J.M., and Gaub H.E. Reversible unfolding of individual titin immunoglobulin domains by AFM. Science 276 (1997) 1109-1112
51. Rief M., Clausen-Schaumann H., and Gaub H.E. Sequence-dependent mechanics of single DNA molecules. Nat. Struct. Biol. 6 (1999) 346-349
52. Root D.D., Yadavalli V.K., Forbes J.G., and Wang K. Coiled-coil nanomechanics and uncoiling and unfolding of the superhelix and alpha-helices of myosin. Biophys. J. 90 (2006) 2852-2866
53. Sarkar A., Caamano S., and Fernandez J.M. The mechanical fingerprint of a parallel polyprotein dimer. Biophys. J. 92 (2007) L36-L38
54. Schwaiger I., Sattler C., Hostetter D.R., and Rief M. The myosin coiled-coil is a truly elastic protein structure. Nat. Mater. 1 (2002) 232-235
55. Smith S.B., Cui Y., and Bustamante C. Overstretching B-DNA: the elastic response of individual double-stranded and single-stranded DNA molecules. Science 271 (1996) 795-799
56. Sotomayor M., and Schulten K. Single-molecule experiments in vitro and in silico. Science 316 (2007) 1144-1148
57. Sotomayor M., Corey D.P., and Schulten K. In search of the hair-cell gating spring elastic properties of ankyrin and cadherin repeats. Structure 13 (2005) 669-682
58. Spraggon G., Everse S.J., and Doolittle R.F. Crystal structures of fragment D from human fibrinogen and its crosslinked counterpart from fibrin. Nature 389 (1997) 455-462
59. Takebe M., Soe G., Kohno I., Sugo T., and Matsuda M. Calcium ion-dependent monoclonal antibody against human fibrinogen: preparation, characterization, and application to fibrinogen purification. Thromb. Haemost. 73 (1995) 662-667
60. Walshaw J., and Woolfson D.N. Socket: a program for identifying and analysing coiled-coil motifs within protein structures. J. Mol. Biol. 307 (2001) 1427-1450
61. Walshaw J., and Woolfson D.N. Extended knobs-into-holes packing in classical and complex coiled-coil assemblies. J. Struct. Biol. 144 (2003) 349-361
62. Weisel J.W. The mechanical properties of fibrin for basic scientists and clinicians. Biophys. Chem. 112 (2004) 267-276
63. Weisel J.W. Fibrinogen and fibrin. Adv. Protein Chem. 70 (2005) 247-299
64. Weisel J.W., Stauffacher C.V., Bullitt E., and Cohen C. A model for fibrinogen: domains and sequence. Science 230 (1985) 1388-1391
65. Yang Z., Kollman J.M., Pandi L., and Doolittle R.F. Crystal structure of native chicken fibrinogen at 2.7 A resolution. Biochemistry 40 (2001) 12515-12523