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BioMed Research International
Volume 2017, Article ID 6385628, 13 pages
https://doi.org/10.1155/2017/6385628
Research Article

Nonuniform Internal Structure of Fibrin Fibers: Protein Density and Bond Density Strongly Decrease with Increasing Diameter

1Department of Physics, Wake Forest University, Winston-Salem, NC 27109, USA
2Leeds Institute of Cardiovascular & Metabolic Medicine, The LIGHT Laboratories, University of Leeds, Clarendon Way, Leeds LS2 9NL, UK
3Department of Physics, University of Richmond, Richmond, VA 23173, USA
4Centre of Excellence for Nutrition, North-West University, Potchefstroom, South Africa
5Department of Health & Exercise Science, Wake Forest University, Winston-Salem, NC 27109, USA
6NanoMedica, LLC, Biotech Place, 575 Patterson Ave, Winston-Salem, NC 27101, USA

Correspondence should be addressed to Martin Guthold; ude.ufw@mdlohtug

Received 22 February 2017; Revised 5 May 2017; Accepted 22 August 2017; Published 10 October 2017

Academic Editor: Jeroen Rouwkema

Copyright © 2017 Wei Li et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. N. Laurens, P. Koolwijk, and M. P. de Maat, “Fibrin structure and wound healing,” Journal of Thrombosis and Haemostasis, vol. 4, no. 5, pp. 932–939, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. R. F. Doolittle, “Fibrinogen and fibrin,” Annual Review of Biochemistry, vol. 53, pp. 195–229, 1983. View at Publisher · View at Google Scholar · View at Scopus
  3. M. W. Mosesson, “Fibrinogen and fibrin structure and functions,” Journal of Thrombosis and Haemostasis, vol. 3, no. 8, pp. 1894–1904, 2005. View at Publisher · View at Google Scholar · View at Scopus
  4. J. H. Brown, N. Volkmann, G. Jun, A. H. Henschen-Edman, and C. Cohen, “The crystal structure of modified bovine fibrinogen,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 1, pp. 85–90, 2000. View at Publisher · View at Google Scholar · View at Scopus
  5. T. Riedel, J. Suttnar, E. Brynda, M. Houska, L. Medved, and J. E. Dyr, “Fibrinopeptides A and B release in the process of surface fibrin formation,” Blood, vol. 117, no. 5, pp. 1700–1705, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. Z. Yang, I. Mochalkin, and R. F. Doolittle, “A model of fibrin formation based on crystal structures of fibrinogen and fibrin fragments complexed with synthetic peptides,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 26, pp. 14156–14161, 2000. View at Publisher · View at Google Scholar · View at Scopus
  7. A. L. C. La Corte, H. Philippou, and R. A. S. Arins, “Role of fibrin structure in thrombosis and vascular disease,” Advances in Protein Chemistry and Structural Biology, vol. 83, pp. 75–127, 2011. View at Publisher · View at Google Scholar · View at Scopus
  8. G. Caracciolo, M. De Spirito, A. C. Castellano et al., “Protofibrils within fibrin fibres are packed together in a regular array,” Thrombosis and Haemostasis, vol. 89, no. 4, pp. 632–636, 2003. View at Google Scholar · View at Scopus
  9. M. Guthold, W. Liu, B. Stephens et al., “Visualization and mechanical manipulations of individual fibrin fibers suggest that fiber cross section has fractal dimension 1.3,” Biophysical Journal, vol. 87, no. 6, pp. 4226–4236, 2004. View at Publisher · View at Google Scholar · View at Scopus
  10. E. B. Hunziker, P. W. Straub, and A. Haeberli, “A new concept of fibrin formation based upon the linear growth of interlacing and branching polymers and molecular alignment into interlocked single-stranded segments,” Journal of Biological Chemistry, vol. 265, no. 13, pp. 7455–7463, 1990. View at Google Scholar · View at Scopus
  11. M. Rocco, M. Molteni, M. Ponassi et al., “A comprehensive mechanism of fibrin network formation involving early branching and delayed single- to double-strand transition from coupled time-resolved X-ray/Light-scattering detection,” Journal of the American Chemical Society, vol. 136, no. 14, pp. 5376–5384, 2014. View at Publisher · View at Google Scholar · View at Scopus
  12. M. E. Carr Jr. and J. Hermans, “Size and density of fibrin fibers from turbidity.,” Macromolecules, vol. 11, no. 1, pp. 46–50, 1978. View at Publisher · View at Google Scholar · View at Scopus
  13. M. E. Carr and D. A. Gabriel, “Dextran-induced changes in fibrin fiber size and density based on wavelength dependence of gel turbidity,” Macromolecules, vol. 13, no. 6, pp. 1473–1477, 1980. View at Publisher · View at Google Scholar · View at Scopus
  14. M. De Spirito, G. Arcòvito, M. Papi, M. Rocco, and F. Ferri, “Small- and wide-angle elastic light scattering study of fibrin structure,” Journal of Applied Crystallography, vol. 36, no. 3 I, pp. 636–641, 2003. View at Publisher · View at Google Scholar · View at Scopus
  15. M. Papi, G. Arcovito, M. De Spirito, G. Amiconi, A. Bellelli, and G. Boumis, “Simultaneous static and dynamic light scattering approach to the characterization of the different fibrin gel structures occurring by changing chloride concentration,” Applied Physics Letters, vol. 86, no. 18, Article ID 183901, pp. 1–3, 2005. View at Publisher · View at Google Scholar · View at Scopus
  16. E. A. Ryan, L. F. Mockros, J. W. Weisel, and L. Lorand, “Structural origins of fibrin clot rheology,” Biophysical Journal, vol. 77, no. 5, pp. 2813–2826, 1999. View at Publisher · View at Google Scholar · View at Scopus
  17. J. W. Weisel, “The mechanical properties of fibrin for basic scientists and clinicians,” Biophysical Chemistry, vol. 112, no. 2-3, pp. 267–276, 2004. View at Publisher · View at Google Scholar · View at Scopus
  18. W. Li, J. Sigley, M. Pieters et al., “Fibrin fiber stiffness is strongly affected by fiber diameter, but not by fibrinogen glycation,” Biophysical Journal, vol. 110, no. 6, pp. 1400–1410, 2016. View at Publisher · View at Google Scholar · View at Scopus
  19. C. C. Helms, R. A. S. Ariëns, S. Uitte De Willige, K. F. Standeven, and M. Guthold, “α-α Cross-links increase fibrin fiber elasticity and stiffness,” Biophysical Journal, vol. 102, no. 1, pp. 168–175, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. W. Liu, C. R. Carlisle, E. A. Sparks, and M. Guthold, “The mechanical properties of single fibrin fibers,” Journal of Thrombosis and Haemostasis, vol. 8, no. 5, pp. 1030–1036, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. C. R. Carlisle, E. A. Sparks, C. Der loughian, and M. Guthold, “Strength and failure of fibrin fiber branchpoints,” Journal of Thrombosis and Haemostasis, vol. 8, no. 5, pp. 1135–1138, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. W. Liu, L. M. Jawerth, E. A. Sparks et al., “Fibrin fibers have extraordinary extensibility and elasticity,” Science, vol. 313, no. 5787, pp. 634–634, 2006. View at Google Scholar
  23. I. Bucay, E. T. O'Brien, S. D. Wulfe et al., “Physical determinants of fibrinolysis in single fibrin fibers,” PLoS ONE, vol. 10, no. 2, Article ID e0116350, 2015. View at Publisher · View at Google Scholar · View at Scopus
  24. J. R. Houser, N. E. Hudson, L. Ping et al., “Evidence that αC region is origin of low modulus, high extensibility, and strain stiffening in fibrin fibers,” Biophysical Journal, vol. 99, no. 9, pp. 3038–3047, 2010. View at Publisher · View at Google Scholar · View at Scopus
  25. N. E. Hudson, J. R. Houser, E. T. O'Brien III et al., “Stiffening of individual fibrin fibers equitably distributes strain and strengthens networks,” Biophysical Journal, vol. 98, no. 8, pp. 1632–1640, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. J.-P. Collet, H. Shuman, R. E. Ledger, S. Lee, and J. W. Weisel, “The elasticity of an individual fibrin fiber in a clot,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 26, pp. 9133–9137, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. M. R. Falvo, D. Millard, E. T. O'Brien III, R. Superfine, and S. T. Lord, “Length of tandem repeats in fibrin's αC region correlates with fiber extensibility,” Journal of Thrombosis and Haemostasis, vol. 6, no. 11, pp. 1991–1993, 2008. View at Publisher · View at Google Scholar · View at Scopus
  28. C. Yeromonahos, B. Polack, and F. Caton, “Nanostructure of the fibrin clot,” Biophysical Journal, vol. 99, no. 7, pp. 2018–2027, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. I. S. Yermolenko, V. K. Lishko, T. P. Ugarova, and S. N. Magonov, “High-resolution visualization of fibrinogen molecules and fibrin fibers with atomic force microscopy,” Biomacromolecules, vol. 12, no. 2, pp. 370–379, 2011. View at Publisher · View at Google Scholar · View at Scopus
  30. J. W. Weisel, “Fibrin assembly. Lateral aggregation and the role of the two pairs of fibrinopeptides,” Biophysical Journal, vol. 50, no. 6, pp. 1079–1093, 1986. View at Publisher · View at Google Scholar · View at Scopus
  31. J. Hermans, “Model of fibrin,” in Proceedings of the National Academy of Sciences of the United States of America, vol. 76, pp. 1189–1193, 1979.
  32. A. D. Protopopova, N. A. Barinov, E. G. Zavyalova, A. M. Kopylov, V. I. Sergienko, and D. V. Klinov, “Visualization of fibrinogen αC regions and their arrangement during fibrin network formation by high-resolution AFM,” Journal of Thrombosis and Haemostasis, vol. 13, no. 4, pp. 570–579, 2015. View at Publisher · View at Google Scholar · View at Scopus
  33. M. Pieters, N. Covic, F. H. Van Der Westhuizen et al., “Glycaemic control improves fibrin network characteristics in type 2 diabetes - A purified fibrinogen model,” Thrombosis and Haemostasis, vol. 99, no. 4, pp. 691–700, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. S. Baker, J. Sigley, C. C. Helms et al., “The mechanical properties of dry, electrospun fibrinogen fibers,” Mater. Sci. Eng. C-Mater. Biol. Appl, vol. 32, no. 2, pp. 215–221, 2012. View at Google Scholar
  35. C. R. Carlisle, C. Coulais, M. Namboothiry, D. L. Carroll, R. R. Hantgan, and M. Guthold, “The mechanical properties of individual, electrospun fibrinogen fibers,” Biomaterials, vol. 30, no. 6, pp. 1205–1213, 2009. View at Publisher · View at Google Scholar · View at Scopus
  36. C. Bustamante and D. Keller, “Scanning Force Microscopy in Biology,” Physics Today, vol. 48, no. 12, pp. 32–38, 1995. View at Publisher · View at Google Scholar · View at Scopus
  37. E. L. Smith, B. Cardinali, L. Ping, R. A. S. Ariëns, and H. Philippou, “Elimination of coagulation factor XIII from fibrinogen preparations,” Journal of Thrombosis and Haemostasis, vol. 11, no. 5, pp. 993–995, 2013. View at Publisher · View at Google Scholar · View at Scopus
  38. N. A. Kurniawan, J. Grimbergen, J. Koopman, and G. H. Koenderink, “Factor XIII stiffens fibrin clots by causing fiber compaction,” Journal of Thrombosis and Haemostasis, vol. 12, no. 10, pp. 1687–1696, 2014. View at Publisher · View at Google Scholar · View at Scopus
  39. J. W. Weisel, “The electron microscope band pattern of human fibrin: Various stains, lateral order, and carbohydrate localization,” Journal of Ultrastructure Research and Molecular Structure Research, vol. 96, no. 1-3, pp. 176–188, 1986. View at Publisher · View at Google Scholar · View at Scopus
  40. S. Bernocco, F. Ferri, A. Profumo, C. Cuniberti, and M. Rocco, “Polymerization of rod-like macromolecular monomers studied by stopped- flow, multiangle light scattering: Set-up, data processing, and application to fibrin formation,” Biophysical Journal, vol. 79, no. 1, pp. 561–583, 2000. View at Publisher · View at Google Scholar · View at Scopus
  41. K. M. Weigandt, D. C. Pozzo, and L. Porcar, “Structure of high density fibrin networks probed with neutron scattering and rheology,” Soft Matter, vol. 5, no. 21, pp. 4321–4330, 2009. View at Publisher · View at Google Scholar · View at Scopus
  42. O. V. Gorkun, A. H. Henschen-Edman, L. F. Ping, and S. T. Lord, “Analysis of Aα251 fibrinogen: The αC domain has a role in polymerization, albeit more subtle than anticipated from the analogous proteolytic fragment X,” Biochemistry, vol. 37, no. 44, pp. 15434–15441, 1998. View at Publisher · View at Google Scholar · View at Scopus
  43. R. I. Litvinov, S. Yakovlev, G. Tsurupa, O. V. Gorkun, L. Medved, and J. W. Weisel, “Direct evidence for specific interactions of the fibrinogen αC-domains with the central E region and with each other,” Biochemistry, vol. 46, no. 31, pp. 9133–9142, 2007. View at Publisher · View at Google Scholar · View at Scopus
  44. G. Tsurupa, R. R. Hantgan, R. A. Burton, I. Pechik, N. Tjandra, and L. Medved, “Structure, stability, and interaction of the fibrin(ogen) αC-domains,” Biochemistry, vol. 48, no. 51, pp. 12191–12201, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. G. Tsurupa, I. Pechik, R. I. Litvinov et al., “On the mechanism of αc polymer formation in fibrin,” Biochemistry, vol. 51, no. 12, pp. 2526–2538, 2012. View at Publisher · View at Google Scholar · View at Scopus
  46. L. Ping, L. Huang, B. Cardinali, A. Profumo, O. V. Gorkun, and S. T. Lord, “Substitution of the human αc region with the analogous chicken domain generates a fibrinogen with severely impaired lateral aggregation: Fibrin monomers assemble into protofibrils but protofibrils do not assemble into fibers,” Biochemistry, vol. 50, no. 42, pp. 9066–9075, 2011. View at Publisher · View at Google Scholar · View at Scopus
  47. H. Song and J. Parkinson, “Modelling the self-assembly of elastomeric proteins provides insights into the evolution of their domain architectures,” PLoS Computational Biology, vol. 8, no. 3, Article ID e1002406, 2012. View at Publisher · View at Google Scholar · View at Scopus
  48. D. J. Curtis, M. R. Brown, K. Hawkins et al., “Rheometrical and molecular dynamics simulation studies of incipient clot formation in fibrin-thrombin gels: An activation limited aggregation approach,” Journal of Non-Newtonian Fluid Mechanics, vol. 166, no. 16, pp. 932–938, 2011. View at Publisher · View at Google Scholar · View at Scopus