Evidence that αC region is origin of low modulus, high extensibility, and strain stiffening in fibrin fibers

Biophysical Journal

Volumn 99, Issue 9, 2010, Pages 3038-3047

  Houser, John R ^a   Hudson, Nathan E ^a   Ping, Lifang ^b   O'Brien III, E Timothy ^a   Superfine, Richard ^a   Lord, Susan T ^b   Falvo, Michael R ^a  

^a University of North Carolina at Chapel Hill   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 78349249820     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2010.08.060     Document Type: Article

References (61)

1. Weisel, J. W. 2004. The mechanical properties of fibrin for basic scientists and clinicians. Biophys. Chem. 112:267-276.
2. Hudson, N. E., J. R. Houser., M. R. Falvo. 2010. Stiffening of individual fibrin fibers equitably distributes strain and strengthens networks. Biophys. J. 98:1632-1640.
3. Liu, W., C. R. Carlisle., M. Guthold. 2010. The mechanical properties of single fibrin fibers. J. Thromb. Haemost. 8:1030-1036.
4. Falvo, M. R., D. Millard., S. T. Lord. 2008. Length of tandem repeats in fibrin's aC region correlates with fiber extensibility. J. Thromb. Haemost. 6:1991-1993.
5. Guthold, M., W. Liu., S. T. Lord. 2007. A comparison of the mechanical and structural properties of fibrin fibers with other protein fibers. Cell Biochem. Biophys. 49:165-181.
6. Liu, W., L. M. Jawerth., M. Guthold. 2006. Fibrin fibers have extraordinary extensibility and elasticity. Science. 313:634.
7. Kang, H., Q. Wen., F. C. Mackintosh. 2009. Nonlinear elasticity of stiff filament networks: strain stiffening, negative normal stress, and filament alignment in fibrin gels. J. Phys. Chem. B. 113:3799-3805.
8. Bale, M. D., and J. D. Ferry. 1988. Strain enhancement of elastic modulus in fine fibrin clots. Thromb. Res. 52:565-572.
9. Shah, J. V., and P. A. Janmey. 1997. Strain hardening of fibrin gels and plasma clots. Rheolog. Acta. 36:262-268.
10. Janmey, P. A., M. E. McCormick., F. C. MacKintosh. 2007. Negative normal stress in semiflexible biopolymer gels. Nat. Mater. 6:48-51.
11. Buehler, M. J. 2006. Nature designs tough collagen: explaining the nanostructure of collagen fibrils. Proc. Natl. Acad. Sci. USA. 103:12285-12290.
12. Buehler, M. J., and Y. C. Yung. 2009. Deformation and failure of protein materials in physiologically extreme conditions and disease. Nat. Mater. 8:175-188.
13. Aizenberg, J., J. C. Weaver., P. Fratzl. 2005. Skeleton of Euplectella sp.: structural hierarchy from the nanoscale to the macroscale. Science. 309:275-278.
14. Lord, S. T. 2007. Fibrinogen and fibrin: scaffold proteins in hemostasis. Curr. Opin. Hematol. 14:236-241.
15. Weisel, J. W. 2005. Fibrinogen and fibrin. Adv. Protein Chem. 70:247-299.
16. Ferry, J. D., and P. R. Morrison. 1944. Chemical, clinical, and immunological studies on the products of human plasma fractionation. XVI. Fibrin clots, fibrin films, and fibrinogen plastics. J. Clin. Invest. 23:566-572.
17. Gerth, C., W. W. Roberts, and J. D. Ferry. 1974. Rheology of fibrin clots. II. Linear viscoelastic behavior in shear creep. Biophys. Chem. 2:208-217.
18. Roberts, W. W., O. Kramer., J. D. Ferry. 1974. Rheology of fibrin clots. I. Dynamic viscoelastic properties and fluid permeation. Biophys. Chem. 1:152-160.
19. Lorand, L. 1950. Fibrin clots. Nature. 166:694-695.
20. Roberts, W. W., L. Lorand, and L. F. Mockros. 1973. Viscoelastic properties of fibrin clots. Biorheology. 10:29-42.
21. Mockros, L. F., W. W. Roberts, and L. Lorand. 1974. Viscoelastic properties of ligation-inhibited fibrin clots. Biophys. Chem. 2:164-169.
22. Ryan, E. A., L. F. Mockros., L. Lorand. 1999. Influence of a natural and a synthetic inhibitor of factor XIIIa on fibrin clot rheology. Biophys. J. 77:2827-2836.
23. Standeven, K. F., A. M. Carter., R. A. Ariëns. 2007. Functional analysis of fibrin gamma-chain cross-linking by activated factor XIII: determination of a cross-linking pattern that maximizes clot stiffness. Blood. 110:902-907.
24. Ariëns, R. A., T. S. Lai., P. J. Grant. 2002. Role of factor XIII in fibrin clot formation and effects of genetic polymorphisms. Blood. 100:743-754.
25. Brown, A. E., R. I. Litvinov., J. W. Weisel. 2007. Forced unfolding of coiled-coils in fibrinogen by single-molecule AFM. Biophys. J. 92: L39-L41.
26. Lim, B. B., E. H. Lee., K. Schulten. 2008. Molecular basis of fibrin clot elasticity. Structure. 16:449-459.
27. Averett, L. E., M. H. Schoenfisch., O. V. Gorkun. 2009. Kinetics of the multistep rupture of fibrin 'A-a' polymerization interactions measured using atomic force microscopy. Biophys. J. 97:2820-2828.
28. Averett, L. E., C. B. Geer., M. H. Schoenfisch. 2008. Complexity of "A-a" knob-hole fibrin interaction revealed by atomic force spectroscopy. Langmuir. 24:4979-4988.
29. Gosline, J., M. Lillie., K. Savage. 2002. Elastic proteins: biological roles and mechanical properties. Philos. Trans. R. Soc. Lond. B Biol. Sci. 357:121-132.
30. Gosline, J. M., P. A. Guerette., K. N. Savage. 1999. The mechanical design of spider silks: from fibroin sequence to mechanical function. J. Exp. Biol. 202:3295-3303.
31. Weisel, J. W. 1986. The electron microscope band pattern of human fibrin: various stains, lateral order, and carbohydrate localization. J. Ultrastruct. Mol. Struct. Res. 96:176-188.
32. Tatham, A. S., and P. R. Shewry. 2002. Comparative structures and properties of elastic proteins. Philos. Trans. R. Soc. Lond. B Biol. Sci. 357:229-234.
33. Binnie, C. G., and S. T. Lord. 1993. The fibrinogen sequences that interact with thrombin. Blood. 81:3186-3192.
34. Gorkun, O. V., Y. I. Veklich., S. T. Lord. 1997. The conversion of fibrinogen to fibrin: recombinant fibrinogen typifies plasma fibrinogen. Blood. 89:4407-4414.
35. Collet, J. P., H. Shuman., J. W. Weisel. 2005. The elasticity of an individual fibrin fiber in a clot. Proc. Natl. Acad. Sci. USA. 102:9133-9137.
36. Brown, A. E., R. I. Litvinov., J. W. Weisel. 2009. Multiscale mechanics of fibrin polymer: gel stretching with protein unfolding and loss of water. Science. 325:741-744.
37. Fowler, W. E., R. R. Hantgan., H. P. Erickson. 1981. Structure of the fibrin protofibril. Proc. Natl. Acad. Sci. USA. 78:4872-4876.
38. Hantgan, R. R., and J. Hermans. 1979. Assembly of fibrin. A light scattering study. J. Biol. Chem. 254:11272-11281.
39. Nelb, G. W., G. W. Kamykowski, and J. D. Ferry. 1980. Kinetics of ligation of fibrin oligomers. J. Biol. Chem. 255:6398-6402.
40. Weisel, J. W., Y. Veklich, and O. Gorkun. 1993. The sequence of cleavage of fibrinopeptides from fibrinogen is important for protofibril formation and enhancement of lateral aggregation in fibrin clots. J. Mol. Biol. 232:285-297.
41. Kellermayer, M. S., S. B. Smith., C. Bustamante. 1997. Folding-unfolding transitions in single titin molecules characterized with laser tweezers. Science. 276:1112-1116.
42. Oberhauser, A. F., P. E. Marszalek., J. M. Fernandez. 1998. The molecular elasticity of the extracellular matrix protein tenascin. Nature. 393:181-185.
43. Rief, M., M. Gautel., H. E. Gaub. 1998. The mechanical stability of immunoglobulin and fibronectin III domains in the muscle protein titin measured by atomic force microscopy. Biophys. J. 75:3008-3014.
44. Rief, M., J. Pascual., H. E. Gaub. 1999. Single molecule force spectroscopy of spectrin repeats: low unfolding forces in helix bundles. J. Mol. Biol. 286:553-561.
45. Schwaiger, I., C. Sattler., M. Rief. 2002. The myosin coiled-coil is a truly elastic protein structure. Nat. Mater. 1:232-235.
46. Bustamante, C., J. F. Marko., S. Smith. 1994. Entropic elasticity of λ-phage DNA. Science. 265:1599-1600.
47. Rief, M., M. Gautel., H. E. Gaub. 1997. Reversible unfolding of individual titin immunoglobulin domains by AFM. Science. 276:1109-1112.
48. Kellermayer, M. S., C. Bustamante, and H. L. Granzier. 2003. Mechanics and structure of titin oligomers explored with atomic force microscopy. Biochim. Biophys. Acta. 1604:105-114.
49. Piechocka, I. K., R. G. Bacabac., G. H. Koenderink. 2010. Structural hierarchy governs fibrin gel mechanics. Biophys. J. 98:2281-2289.
50. Sobel, J. H., and M. A. Gawinowicz. 1996. Identification of the a-chain lysine donor sites involved in factor XIIIa fibrin cross-linking. J. Biol. Chem. 271:19288-19297.
51. Litvinov, R. I., S. Yakovlev., J. W. Weisel. 2007. Direct evidence for specific interactions of the fibrinogen aC-domains with the central E region and with each other. Biochemistry. 46:9133-9142.
52. Marko, J. F., and E. D. Siggia. 1995. Statistical mechanics of supercoiled DNA. Phys. Rev. E. 52:2912-2938.
53. Miserez, A., S. S. Wasko., J. H. Waite. 2009. Non-entropic and reversible long-range deformation of an encapsulating bioelastomer. Nat. Mater. 8:910-916.
54. Hearle, J. W. 2000. A critical review of the structural mechanics of wool and hair fibers. Int. J. Biol. Macromol. 27:123-138.
55. Qin, Z., L. Kreplak, and M. J. Buehler. 2009. Hierarchical structure controls nanomechanical properties of vimentin intermediate filaments. PLoS ONE. 4: e7294.
56. Kreplak, L., and D. Fudge. 2007. Biomechanical properties of intermediate filaments: from tissues to single filaments and back. Bioessays. 29:26-35.
57. Fudge, D. S., and J. M. Gosline. 2004. Molecular design of the a-keratin composite: insights from a matrix-free model, hagfish slime threads. Proc. Biol. Sci. 271:291-299.
58. Fudge, D. S., K. H. Gardner., J. M. Gosline. 2003. The mechanical properties of hydrated intermediate filaments: insights from hagfish slime threads. Biophys. J. 85:2015-2027.
59. Rief, M., M. Gautel, and H. E. Gaub. 2000. Unfolding forces of titin and fibronectin domains directly measured by AFM. Adv. Exp. Med. Biol. 481:129-141.
60. Ryan, E. A., L. F. Mockros., L. Lorand. 1999. Structural origins of fibrin clot rheology. Biophys. J. 77:2813-2826.
61. Treloar, L. R. G. 1944. Stress-strain data for vulcanized rubber under various types of deformation. Trans. Faraday Soc. 40:59-70.