Structural hierarchy governs fibrin gel mechanics

Biophysical Journal

Volumn 98, Issue 10, 2010, Pages 2273-2280

  Piechocka, Izabela K ^a   Bacabac, Rommel G ^a   Potters, Max ^b   MacKintosh, Fred C ^b   Koenderink, Gijsje H ^a  

^a FOM INSTITUTE AMOLF   (Netherlands)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 77952787332     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2010.01.052     Document Type: Article

References (67)

1. Laurens, N., P. Koolwijk, and M. D. Maat. 2008. Fibrin structure and wound healing. J. Thromb. Haemost. 4:932-939.
2. Kroll, M. H., J. D. Heliums, ..., J. L. Moake. 1996. Platelets and shear stress. Blood. 88:1525-1541.
3. Shah, J., and P. Janmey. 1997. Strain, hardening of fibrin, gels and plasma clots. Rheol. Acta. 36:262-268. (Pubitemid 127630991)
4. Liu, W., L. M. Jawerth, ..., M. Guthold. 2006. Fibrin fibers have extraordinary extensibility and elasticity. Science. 313:634-638. (Pubitemid 44201134)
5. Brown, A. E. X., 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.
6. Wen, Q., A. Basu, ..., P. Janmey. 2007. Local and global deformations in a strain-stiffening fibrin gel. N. J. Phys. 9:428-1 - 428-510 (Pubitemid 350241873)
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. Roberts, W. W., L. Lorand, and L. F. Mockros. 1973. Viscoelastic properties of fibrin clots. Biorheology. 10:29-42.
9. Yao, N., R. J. Larsen, and D. Weitz. 2008. Probing nonlinear rheology with inertio-elastic oscillations. J. Rheol. (N. Y. N. Y.). 52:1013-1025.
10. Janmey, P., E. Amis, and J. Ferry. 1983. Rheology of fibrin clots. VI. Stress relaxation, creep, and differential dynamic modulus of fine clots in large shearing deformations. J. Rheol. (N. Y. N. Y.). 27:135-153. (Pubitemid 13526237)
11. Standeven, K. F., R. A. Ariens, and P. J. Grant. 2005. The molecular physiology and pathology of fibrin structure/function. Blood Rev. 19:275-288.
12. Weisel, J. W. 2008. Biophysics. Enigmas of blood clot elasticity. Science. 320:456-457.
13. - regulates the structure of the fibrin clot. Biophys. J. 75:1973-1979.
14. 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.
15. Roska, F. J., and J. D. Ferry. 1982. Studies of fibrin film. I. Stress relaxation and birefringence. Biopolymers. 21:1811-1832. (Pubitemid 13253076)
16. Onck, P. R., T. Koeman, ..., E. van der Giessen. 2005. Alternative explanation of stiffening in cross-linked semiflexible networks. Phys. Rev. Lett. 95:178102.
17. Conti, E., and F. C. Mackintosh. 2009. Cross-linked networks of stiff filaments exhibit negative normal stress. Phys. Rev. Lett. 102:088102.
18. Heussinger, C., M. Bathe, and E. Frey. 2007. Statistical mechanics of semiflexible bundles of wormlike polymer chains. Phys. Rev. Lett. 99:048101. (Pubitemid 47173169)
19. Fowler, W., R. Hantgan, ..., H. Erickson. 1978. Structure of the fibrin protofibril. Proc. Natl. Acad. Sci. USA. 1981:4872-4876.
20. Ferry, J., and P. Morrison. 1947. Preparation and properties of serum and plasma proteins. VIII. The conversion of human fibrinogen to fibrin under various conditions. J. Am. Chem. Soc. 69:388-400.
21. Yang, Z., J. M. Kollman, ...., R. F. Doolittle. 200.1, Crystal, structure of native chicken, fibrinogen at 2.7 Å resolution. Biochemistry. 40: 12515-12523.
22. Carr, Jr., M. E., and J. Hermans. 1978. Size and density of fibrin fibers from turbidity. Macromolecules. 11:46-50.
23. Guthold, M., W. Liu, ..., R. Superfine. 2004. Visualization and mechanical manipulations of individual fibrin fibers suggest that fiber cross section has fractal dimension 1.3. Biophys. J. 87:4226-4236. (Pubitemid 39602925)
24. Voter, W. A., C. Lucaveche, and H. P. Erickson. 1986. Concentration of protein in fibrin fibers and fibrinogen polymers determined by refractive index matching. Biopolymers. 25:2375-2384.
25. Claessens, M. M., M. Bathe,..., A. R. Bausch. 2006. Actin-bindingproteins sensitively mediate F-actin bundle stiffness. Nat. Mater. 5:748-753.
26. Gorkun, O. V., Y. I. Veklich, ..., J. W. Weisel. 1994. Role of the αC domains of fibrin in clot formation. Biochemistry. 33:6986-6997. (Pubitemid 2102270)
27. Collet, J. P., J. L. Moen, ...., J. W. Weisel. 2005. The αC domains of fibrinogen affect the structure of the fibrin clot, its physical properties, and its susceptibility to fibrinolysis. Blood. 106:3824-3830.
28. Litvinov, R. I., S. Yakovlev, ..., J. W. Weisel. 2007. Direct evidence for specific interactions of the fibrinogen αC-domains with the central E region and with each other. Biochemistry. 46:9133-9142.
29. Weisel, J. W., and L. Medved. 2001. The structure and function of the αC domains of fibrinogen. Ann. N. Y. Acad. Sci. 936:312-327.
30. Doolittle, R. F., and J. M. Kollman. 2006. Natively unfolded regions of the vertebrate fibrinogen molecule. Proteins. 63:391-397.
31. Storm, C., J. J. Pastore, ..., P. A. Janmey. 2005. Nonlinear elasticity in biological gels. Nature. 435:191-194.
32. MacKintosh, F. C., J. Käs, and P. A. Janmey. 1995. Elasticity of semiflexible biopolymer networks. Phys. Rev. Lett. 75:4425-4428.
33. Gardel, M. L., J. H. Shin, ..., D. A. Weitz. 2004. Elastic behavior of cross-linked and bundled actin networks. Science. 304:1301-1305.
34. Bendix, P. M., G. H. Koenderink, ..., D. A. Weitz. 2008. A quantitative analysis of contractility in active cytoskeletal protein networks. Biophys. J. 94:3126-3136.
35. Koenderink, G. H., M. Atakhorrami, ..., C. F. Schmidt. 2006. Highfrequency stress relaxation in semiflexible polymer solutions and networks. Phys. Rev. Lett. 96:138307.
36. Gittes, F., B. Schnurr, ..., C. Schmidt. 1997. Microscopic viscoelas- ticity: shear moduli of soft materials determined from thermal fluctuations. Phys. Rev. Lett. 17:3286-3289. (Pubitemid 127624769)
37. Nelb, G. W., C. Gerth, and J. D. Ferry. 1976. Rheology of fibrin clots. III. Shear creep and creep recovery of fine ligated and coarse unligated clots. Biophys. Chem. 5:377-387.
38. 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.
39. Gittes, F., and F. MacKintosh. 1998. Dynamic shear modulus of a semiflexible polymer network. Phys. Rev. E Stat. Phys. Plasmas Fluids Relat. Interdiscip. Topics. 58:R1241-R1244. (Pubitemid 128596172)
40. Morse, D. 1998. Viscoelasticity of tightly entangled solutions of semiflexible polymers. Phys. Rev. E Stat. Phys. Plasmas Fluids Relat. Interdiscip. Topics. 58:R1237-R1240. (Pubitemid 128596171)
41. Willenbacher, N., C. Oelschlaeger, ..., F. Scheffold. 2007. Broad bandwidth optical and mechanical rheometry of wormlike micelle solutions. Phys. Rev. Lett. 99:068302. (Pubitemid 47263131)
42. Granek, R. 1997. From semi-flexible polymers to membranes: anomalous diffusion and reptation. J. Phys. II. 7:1761-1788. (Pubitemid 127806180)
43. Shen, L. L., J. Hermans, ..., M. Carr. 1975. Effects of calcium, ion and covalentcrosslinking on formation and elasticity of fibrin cells. Thromb. Res. 6:255-265.
44. Fukada, E., and M. Kaibara. 1973. The dynamic rigidity of fibrin gels. Biorheology. 10:129-138.
45. Satcher, Jr., R. L., and C. F. Dewey, Jr. 1996. Theoretical estimates of mechanical properties of the endothelial cell cytoskeleton. Biophys. J. 71:109-118.
46. Kroy, K., and E. Frey. 1996. Force-extension relation and plateau modulus for wormlike chains. Phys. Rev. Lett. 77:306-309. (Pubitemid 126624481)
47. Huisman, E. M., C. Storm, and G. T. Barkema. 2008. Monte Carlo study of multipally crosslinked semiflexible polymer networks. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 78:051801.
48. Jahnel, M., T. A. Waigh, and J. R. Lu. 2008. Thermal fluctuations of fibrin fibers at short time scales. Soft Matter. 4:1438-1442.
49. Sharma, R. C., A. Papagiannopoulos, and T. A. Waigh. 2008. Optical coherence tomography picorheology of biopolymer solutions. Appl. Phys. Lett. 92:173-903.
50. 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.
51. Nunes, C. R., M. T. Roedersheimer, ..., M. W. Luttges. 1995. Effect of microgravity, temperature, and concentration on fibrin and collagen assembly. Microgravity Sci. Technol. 8:125-130.
52. Kaibara, M., E. Fukada, and K. Sakaoku. 1981, Rheological study on network structure of fibrin clots under various conditions. Biorheology. 18:23-35. (Pubitemid 11038309)
53. Bustamante, C., J. F. Marko, ..., S. Smith. 1994. Entropie elasticity of A-phage DNA. Science, 265:1599-1600.
54. Fixman, M., and J. Kovac. 1973. Polymer conformational statistics. III. Modified Gaussian models of stiff chains. J. Chem. Phys. 58:1564-1568.
55. Odijk, T. 1986. The statistics and dynamics of confined or entangled stiff polymers. Macromolecules. 16:1340-1344.
56. Falvo, M. R., D. Millard, ..., S. T. Lord. 2008. Length of tandem repeats in fibrin's αC region, correlates with, fiber extensibility. J. Thromb. Haemost. 6:1991-1993.
57. Bailey, K., W. T. Astbury, and K. M. Rudall. 1943. Fibrinogen and fibrin as a members of the keratin-myosin group. Nature. 151:716-717.
58. Lim, B. B. C., E. H. Lee, ..., K. Schulten. 2008. Molecular basis of fibrin clot elasticity. Structure. 16:449-459.
59. Brown, A. E. X., R. I. Litvinov, ..., J. W. Weisel. 2007. Forced unfolding of coiled-coils in fibrinogen by single-molecule AFM. Biophys. J. 92:L39-L41.
60. Lin, Y., G. Koenderink, ..., D. Weitz. 2007. Viscoelastic properties of microtubule networks. Macromolecules. 40:7714-7720.
61. 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.
62. Litvinov, R. I., O. V. Gorkun, ..., J. W. Weisel. 2007. Polymerization of fibrin: direct observation and quantification of individual B:b knob-hole interactions. Blood. 109:130-138.
63. Standeven, K. F., A. M. Carter, ..., R. A. Ariëns. 2007. Functional analysis of fibrin. γ-chain cross-linking by activated factor XIII: determination of a cross-linking pattern that maximizes clot stiffness. Blood. 110:902-907.
64. Buehler, M. J. 2006. Nature designs tough collagen; explaining the nanostructure of collagen fibrils. Proc. Natl. Acad. Sci, USA. 103:12285-12290.
65. Kreplak, L., H. Bär, ..., U. Aebi. 2005. Exploring the mechanical behavior of single intermediate filaments. J. Mol. Biol. 354:569-577. (Pubitemid 41628276)
66. Janmey, P. A., J. P. Winer, and J. W. Weisel. 2009. Fibrin gels and their clinical and bioengineering applications. J. R. Soc. Interface. 6:1-10.
67. Soon, A. S. C., S. E. Stabenfeldt, ..., T. H. Barker. 2010. Engineering fibrin matrices: the engagement of polymerization pockets through fibrin knob technology for the delivery and retention of therapeutic proteins. Biomaterials. 31:1944-1954.