Fibrin gels and their clinical and bioengineering applications

Journal of the Royal Society Interface

Volumn 6, Issue 30, 2009, Pages 1-10

  Janmey, Paul A ^a,b   Winer, Jessamine P ^b   Weisel, John W ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Elasticity; Extracellular matrix; Fibrin; Gel; Tissue engineering

Indexed keywords

BIOLOGICAL MATERIALS; BIOMECHANICS; COAGULATION; CYTOLOGY; ELASTICITY; FORMING; GELATION; GELS; MECHANICAL PROPERTIES; MONOMERS; POLYMERS; SYNCHROTRONS; TISSUE; TISSUE ENGINEERING;

BIO-CHEMICALS; BIOENGINEERING APPLICATIONS; BLOOD CLOTTING; CELL MIGRATIONS; EXTRACELLULAR MATRIX; FIBRIN; FIBRIN GELS; FIBRIN NETWORKS; GELATION TIMES; NONLINEAR ELASTICITIES; PHYSIOLOGICAL CONDITIONS; POLYMERIZATION MECHANISMS; REACTION CONDITIONS; SMALL STRAINS; SOFT SUBSTRATES;

COLLOIDS;

FIBRIN; FIBRIN GLUE; FIBRIN MONOMER; FIBRINOGEN; HEMOSTATIC AGENT; THROMBIN;

BLEEDING; CELL DIFFERENTIATION; CELL MIGRATION; COMPLIANCE (PHYSICAL); DRUG DELIVERY SYSTEM; ELASTICITY; ELECTRON MICROSCOPY; FIBRIN POLYMERIZATION; FLOW KINETICS; GEL; GELATION; HEMOSTASIS; HUMAN; HYDROGEL; NERVE INJURY; NEURALGIA; PROTEIN STRUCTURE; REVIEW; SKIN FIBROBLAST; TISSUE ENGINEERING; WOUND HEALING; YOUNG MODULUS;

EID: 57349147751     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2008.0327     Document Type: Review

References (93)

1. Albala, D. M. & Lawson, J. H. 2006 Recent clinical and investigational applications of fibrin sealant in selected surgical specialties. J. Am. College Surg. 202, 685-697. (doi:10.1016/j.jamcollsurg. 2005.11.027)
2. Altieri, D. C., Agbanyo, F. R., Plescia, J., Ginsberg, M. H., Edgington, T. S. & Plow, E. F. 1990 A unique recognition site mediates the interaction of fibrinogen with the leukocyte integrin Mac-1 (CD11b/CD18). J. Biol. Chem. 265, 12119-12122.
3. Andree, C. et al. 2008 Improved safety of autologous breast reconstruction surgery by stabilisation of microsurgical vessel anastomoses using fibrin sealant in 349 free DIEP or fascia-muscle-sparing (fms)-TRAM flaps: a twocentre study. Breast 17, 492-498. (doi:10.1016/j.breast. 2008.03.010)
4. Ariëns, R. A. S., Lai, T.-S., Weisel, J. W., Greenberg, C. S. & Grant, P. J. 2002 Role of factor XIII in fibrin clot formation and effects of genetic polymorphisms. Blood 100, 743-754. (doi:10.1182/blood. V100.3.743)
5. Arkudas, A., Tjiawi, J., Bleiziffer, O., Grabinger, L., Polykandriotis, E., Beier, J. P., Sturzl, M., Horch, R. E. & Kneser, U. 2007 Fibrin gel-immobilized VEGF and bFGF efficiently stimulate angiogenesis in the AV loop model. Mol. Med. 13, 480-487. (doi:10.2119/2007-00057.Arkudas)
6. Bach, T. L., Barsigian, C., Chalupowicz, D. G., Busler, D., Yaen, C. H., Grant, D. S. & Martinez, J. 1998 VE-Cadherin mediates endothelial cell capillary tube formation in fibrin and collagen gels. Exp. Cell Res. 238, 324-334. (doi:10.1006/excr.1997.3844)
7. Bhang, S. H., Jeon, O., Choi, C. Y., Kwon, Y. H. & Kim, B. S. 2007 Controlled release of nerve growth factor from fibrin gel. J. Biomed. Mater. Res. A 80, 998-1002.
8. Bjarkam, C. R., Jorgensen, R. L., Jensen, K. N., Sunde, N. A. & Sørensen, J. C. 2007 Deep brain stimulation electrode anchoring using BioGlue®, a protective electrode covering, and a titanium microplate. J. Neurosci. Methods 168, 151-155. (doi:10.1016/j.jneumeth.2007.09.008)
9. Blange, T., van der Heide, U. A., Treijtel, B. W. & de Beer, E. L. 1997 The effect of actin filament compliance on the interpretation of the elastic properties of skeletal muscle fibres. J. Muscle Res. Cell Motil. 18, 125-131. (doi:10.1023/A:1018649420778)
10. Brown, L. F., Lanir, N., McDonagh, J., Tognazzi, K., Dvorak, A. M. & Dvorak, H. F. 1993 Fibroblast migration in fibrin gel matrices. Am. J. Pathol. 142, 273-283.
11. Brown, A. E., Litvinov, R. I., Discher, D. E. & Weisel, J. W. 2007 Forced unfolding of coiled-coils in fibrinogen by single-molecule AFM. Biophys. J. 92, L39-L41. (doi:10.1529/biophysj.106.101261)
12. Buchta, C., Dettke, M., Funovics, P. T., Hirschl, A. M., Macher, M., Worel, N. & Hocker, P. 2004 Impact of manufacturing, irradiation and filtration steps to bacterial contamination of autologous fibrin sealant. Biologicals 32, 165-169. (doi:10.1016/j.biologicals.2004.03.004)
13. Buchta, C., Hedrich, H. C., Macher, M., Hocker, P. & Redl, H. 2005 Biochemical characterization of autologous fibrin sealants produced by CryoSeal and Vivostat in comparison to the homologous fibrin sealant product Tissucol/Tisseel. Biomaterials 26, 6233-6241. (doi:10.1016/j. biomaterials.2005.04.014)
14. Campbell, P. G., Miller, E. D., Fisher, G. W., Walker, L. M. & Weiss, L. E. 2005 Engineered spatial patterns of FGF-2 immobilized on fibrin direct cell organization. Biomaterials 26, 6762-6770. (doi:10.1016/j.biomaterials.2005.04.032)
15. Catelas, I., Sese, N., Wu, B. M., Dunn, J. C., Helgerson, S. & Tawil, B. 2006 Human mesenchymal stem cell proliferation and osteogenic differentiation in fibrin gels in vitro. Tissue Eng. 12, 2385-2396. (doi:10.1089/ten.2006.12.2385)
16. Cheresh, D. A., Berliner, S. A., Vicente, V. & Ruggeri, Z. M. 1989 Recognition of distinct adhesive sites on fibrinogen by related integrins on platelets and endothelial cells. Cell 58, 945-953. (doi:10.1016/0092-8674(89)90946-X)
17. Chernousov, M. A. & Carey, D. J. 2003 αVβ8 integrin is a Schwann cell receptor for fibrin. Exp. Cell Res. 291, 514-524. (doi:10.1016/S0014-4827(03)00409-9)
18. Christman, K. L., Vardanian, A. J., Fang, Q., Sievers, R. E., Fok, H. H. & Lee, R. J. 2004 Injectable fibrin scaffold improves cell transplant survival, reduces infarct expansion, and induces neovasculature formation in ischemic myocardium. J. Am. Coll. Cardiol. 44, 654-660. (doi:10.1016/j.jacc.2004.04.040)
19. Chtcheglova, L. A., Haeberli, A. & Dietler, G. 2008 Force spectroscopy of the fibrin(ogen)-fibrinogen interaction. Biopolymers 89, 292-301. (doi:10.1002/bip.20910)
20. Ciano, P. S., Colvin, R. B., Dvorak, A. M., McDonagh, J. & Dvorak, H. F. 1986 Macrophage migration in fibrin gel matrices. Lab. Invest 54, 62-70.
21. Cohen, I., Gabbay, J., Glaser, T. & Oplatka, A. 1975 Fibrin-blood platelet interaction in a contracting clot. Br. J. Haematol. 31, 45-50. (doi:10.1111/j.1365-2141.1975.tb00830.x)
22. Collet, J. P., Shuman, H., Ledger, R. E., Lee, S. & Weisel, J. W. 2005 The elasticity of an individual fibrin fiber in a clot. Proc. Natl Acad. Sci. USA 102, 9133-9137. (doi:10.1073/pnas.0504120102)
23. Didonna, B. & Lubensky, T. 2005 Nonaffinity and nonlinearity in random elastic networks. Phys. Rev. E 72, 066 619. (doi:10.1103/PhysRevE.72.066619)
24. - regulates the structure of the fibrin clot. Biophys. J. 75, 1973-1979.
25. Dragoo, J. L., Carlson, G., McCormick, F., Khan-Farooqi, H., Zhu, M., Zuk, P. A. & Benhaim, P. 2007 Healing full-thickness cartilage defects using adipose-derived stem cells. Tissue Eng. 13, 1615-1621. (doi:10.1089/ten.2006.0249)
26. Dubey, N., Letourneau, P. C. & Tranquillo, R. T. 2001 Neuronal contact guidance inmagnetically aligned fibrin gels: effect of variation in gel mechano-structural properties. Biomaterials 22, 1065-1075. (doi:10.1016/S0142-9612(00)00341-0)
27. Engler, A. J., Griffin, M. A., Sen, S., Bonnemann, C. G., Sweeney, H. L. & Discher, D. E. 2004 Myotubes differentiate optimally on substrates with tissue-like stiffness: pathological implications for soft or stiff microenvironments. J. Cell Biol. 166, 877-887. (doi:10.1083/jcb.200405004)
28. Eyrich, D., Brandl, F., Appel, B., Wiese, H., Maier, G., Wenzel, M., Staudenmaier, R., Goepferich, A. & Blunk, T. 2007 Long-termstable fibrin gels for cartilage engineering. Biomaterials 28, 55-65. (doi:10.1016/j.biomaterials.2006.08.027)
29. Ferry, J. D. & Morrison, P. R. 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. (doi:10.1021/ja01194a066)
30. Flanagan, T. C., Cornelissen, C., Koch, S., Tschoeke, B., Sachweh, J. S., Schmitz-Rode, T. & Jockenhoevel, S. 2007 The in vitro development of autologous fibrin-based tissue-engineered heart valves through optimised dynamic conditioning. Biomaterials 28, 3388-3397. (doi:10.1016/j.biomaterials.2007.04.012)
31. Galla, T. J., Vedecnik, S. V., Halbgewachs, J., Steinmann, S., Friedrich, C. & Stark, G. B. 2004 Fibrin/Schwann cell matrix in poly-epsilon- caprolactone conduits enhances guided nerve regeneration. Int. J. Artif. Organs 27, 127-136.
32. Gittes, F., Mickey, B., Nettleton, J. & Howard, J. 1993 Flexural rigidity of microtubules and actin filaments measured from thermal fluctuations in shape. J. Cell Biol. 120, 923-934. (doi:10.1083/jcb.120.4.923)
33. Gorodetsky, R., Clark, R. A., An, J., Gailit, J., Levdansky, L., Vexler, A., Berman, E. & Marx, G. 1999 Fibrin microbeads (FMB) as biodegradable carriers for culturing cells and for accelerating wound healing. J. Invest. Dermatol. 112, 866-872. (doi:10.1046/j.1523-1747.1999.00600.x)
34. Guthold, M., Liu, W., Sparks, E. A., Jawerth, L. M., Peng, L., Falvo, M., Superfine, R., Hantgan, R. R. & Lord, S. T. 2007 Acomparison of the mechanical and structural properties of fibrin fibers with other protein fibers. Cell Biochem. Biophys. 49, 165-181. (doi:10.1007/s12013-007-9001- 4)
35. Heussinger, C., Schaefer, B. & Frey, E. 2007 Nonaffine rubber elasticity for stiff polymer networks. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 76, 031 906. (doi:10.1103/PhysRevE.76.031906)
36. Horch, R. E., Bannasch, H., Kopp, J., Andree, C. & Stark, G. B. 1998 Single-cell suspensions of cultured human keratinocytes in fibrin-glue reconstitute the epidermis. Cell Transplant. 7, 309-317. (doi:10.1016/S0963-6897(98) 00005-0)
37. Horch, R. E., Bannasch, H. & Stark, G. B. 2001 Transplantation of cultured autologous keratinocytes in fibrin sealant biomatrix to resurface chronic wounds. Transplant. Proc. 33, 642-644. (doi:10.1016/S0041-1345(00) 02181-3)
38. Huisman, E. M., van Dillen, T., Onck, P. R. & Van der Giessen, E. 2007 Three-dimensional cross-linked F-actin networks: relation between network architecture and mechanical behavior. Phys. Rev. Lett. 99, 208 103. (doi:10.1103/PhysRevLett.99.208103)
39. Janmey, P. A. 1982 Kinetics of formation of fibrin oligomers. I. Theory. Biopolymers 21, 2253-2264. (doi:10.1002/bip.360211112)
40. Janmey, P. A. & Ferry, J. D. 1986 Gel formation by fibrin oligomers without addition of monomers. Biopolymers 25, 1337-1344. (doi:10.1002/bip.360250712)
41. Janmey, P. A., Amis, E. & Ferry, J. 1983 Rheology of fibrin clots. VI. Stress relaxation, creep and differential dynamic modulus of fine clots in large shearing deformations. J. Rheol. 27, 135-153. (doi:10.1122/1.549722)
42. Janmey, P. A., McCormick, M. E., Rammensee, S., Leight, J. L., Georges, P. C. & Mackintosh, F. C. 2007 Negative normal stress in semiflexible biopolymer gels. Nat. Mater. 6, 48-51. (doi:10.1038/nmat1810)
43. Jockenhoevel, S., Zund, G., Hoerstrup, S. P., Chalabi, K., Sachweh, J. S., Demircan, L., Messmer, B. J. & Turina, M. 2001 Fibrin gel - advantages of a new scaffold in cardiovascular tissue engineering. Eur. J. Cardiothorac. Surg. 19, 424-430. (doi:10.1016/S1010-7940(01)00624-8)
44. Kneser, U., Voogd, A., Ohnolz, J., Buettner, O., Stangenberg, L., Zhang, Y. H., Stark, G. B. & Schaefer, D. J. 2005 Fibrin gel-immobilized primary osteoblasts in calcium phosphate bone cement: in vivo evaluation with regard to application as injectable biological bone substitute. Cells Tissues Organs 179, 158-169. (doi:10.1159/000085951)
45. Kuntamukkula, M. S., McIntire, L. V., Moake, J. L., Peterson, D. M. & Thompson, W. J. 1978 Rheological studies of the contractile force within platelet-fibrin clots: effects of prostaglandin E1, dibutyryl-cAMP and dibutyryl-cGMP. Thromb. Res. 13, 957-969. (doi:10.1016/0049- 3848(78)90225-6)
46. Laurens, N., Koolwijk, P. & de Maat, M. P. 2006 Fibrin structure and wound healing. J. Thromb. Haemost. 4, 932-939. (doi:10.1111/j.1538-7836.2006.01861.x)
47. 2 in the γ C-domain of fibrinogen. Biochemistry 41, 12 942-12 951. (doi:10.1021/bi026324c)
48. Litvinov, R. I., Gorkun, O. V., Owen, S. F., Shuman, H. & Weisel, J. W. 2005 Polymerization of fibrin: specificity, strength, and stability of knob-hole interactions studied at the single-molecule level. Blood 106, 2944-2951. (doi:10.1182/blood-2005-05-2039)
49. Liu, W., Jawerth, L. M., Sparks, E. A., Falvo, M. R., Hantgan, R. R., Superfine, R., Lord, S. T. & Guthold, M. 2006 Fibrin fibers have extraordinary extensibility and elasticity. Science 313, 634. (doi:10.1126/science.1127317)
50. Lobb, R., Sasse, J., Sullivan, R., Shing, Y., D'Amore, P., Jacobs, J. & Klagsbrun, M. 1986 Purification and characterization of heparin-binding endothelial cell growth factors. J. Biol. Chem. 261, 1924-1928.
51. Lorand, L. & Graham, R. 2003 Transglutaminases: cross-linking enzymes with pleiotropic functions. Nat. Rev. Mol. Cell. Biol. 4, 140-156. (doi:10.1038/nrm1014)
52. Lord, S. T. 2007 Fibrinogen and fibrin: scaffold proteins in hemostasis. Curr. Opin. Hematol. 14, 236-241. (doi:10.1097/MOH. 0b013e3280dce58c)
53. MacKintosh, F. C., Kas, J. & Janmey, P. A. 1995 Elasticity of semiflexible biopolymer networks. Phys. Rev. Lett. 75, 4425-4428. (doi:10.1103/PhysRevLett.75.4425)
54. Martins, R. S., Siqueira, M. G., Da Silva, C. F. & Plese, J. P. 2005 Overall assessment of regeneration in peripheral nerve lesion repair using fibrin glue, suture, or a combination of the 2 techniques in a rat model. Which is the ideal choice? Surg. Neurol. 64(Suppl. 1), 10-16. (doi:10.1016/j.surneu.2005.04.022)
55. Matsumoto, T., Sasaki, J., Alsberg, E., Egusa, H., Yatani, H. & Sohmura, T. 2007 Three-dimensional cell and tissue patterning in a strained fibrin gel system. PLoS ONE 2, e1211. (doi:10.1371/journal.pone. 0001211)
56. Mazlyzam, A. L., Aminuddin, B. S., Fuzina, N. H., Norhayati, M. M., Fauziah, O., Isa, M. R., Saim, L. & Ruszymah, B. H. 2007 Reconstruction of living bilayer human skin equivalent utilizing human fibrin as a scaffold. Burns 33, 355-363. (doi:10.1016/j.burns.2006.08.022)
57. McManus, M. C., Boland, E. D., Koo, H. P., Barnes, C. P., Pawlowski, K. J., Wnek, G. E., Simpson, D. G. & Bowlin, G. L. 2006 Mechanical properties of electrospun fibrinogen structures. Acta Biomater. 2, 19-28. (doi:10.1016/j.actbio.2005.09.008)
58. McManus, M. C., Boland, E. D., Simpson, D. G., Barnes, C. P. & Bowlin, G. L. 2007 Electrospun fibrinogen: feasibility as a tissue engineering scaffold in a rat cell culture model. J. Biomed. Mater. Res. A 81, 299-309. (doi:10.1002/jbm.a.30989)
59. Miller, E. D., Fisher, G. W., Weiss, L. E., Walker, L. M. & Campbell, P. G. 2006 Dose-dependent cell growth in response to concentration modulated patterns of FGF-2 printed on fibrin. Biomaterials 27, 2213-2221. (doi:10.1016/j.biomaterials.2005.10.021)
60. Mittermayr, R., Wassermann, E., Thurnher, M., Simunek, M. & Redl, H. 2006 Skin graft fixation by slow clotting fibrin sealant applied as a thin layer. Burns 32, 305-311. (doi:10.1016/j.burns.2005.10.010)
61. Mizushima-Sugano, J., Maeda, T. & Miki-Noumura, T. 1983 Flexural rigidity of singlet microtubules estimated from statistical analysis of their contour lengths and end-to-end distances. Biochim. Biophys. Acta 755, 257-262. (doi:10.1016/0304-4165(83)90212-x)
62. Mol, A., van Lieshout, M. I., Dam-de Veen, C. G., Neuenschwander, S., Hoerstrup, S. P., Baaijens, F. P. & Bouten, C. V. 2005 Fibrin as a cell carrier in cardiovascular tissue engineering applications. Biomaterials 26, 3113-3121. (doi:10.1016/j.biomaterials.2004.08.007)
63. Mosesson, M. W. 2005 Fibrinogen and fibrin structure and functions. J. Thromb. Haemost. 3, 1894-1904. (doi:10.1111/j.1538-7836.2005.01365. x)
64. Nehls, V. & Herrmann, R. 1996 The configuration of fibrin clots determines capillary morphogenesis and endothelial cell migration. Microvasc. Res. 51, 347-364. (doi:10.1006/mvre.1996.0032)
65. Nehls, V., Herrmann, R. & Huhnken, M. 1998 Guided migration as a novel mechanism of capillary network remodeling is regulated by basic fibroblast growth factor. Histochem. Cell Biol. 109, 319-329. (doi:10.1007/s004180050232)
66. Odrljin, T. M., Francis, C. W., Sporn, L. A., Bunce, L. A., Marder, V. J. & Simpson-Haidaris, P. J. 1996 Heparin-binding domain of fibrin mediates its binding to endothelial cells. Arterioscler. Thromb. Vasc. Biol. 16, 1544-1551.
67. Onck, P. R., Koeman, T., van Dillen, T. & van der Giessen, E. 2005 Alternative explanation of stiffening in cross-linked semiflexible networks. Phys. Rev. Lett. 95, 178 102. (doi:10.1103/PhysRevLett.95.178102)
68. Park, S. H., Park, S. R., Chung, S. I., Pai, K. S. & Min, B. H. 2005 Tissue-engineered cartilage using fibrin/hyaluronan composite gel and its in vivo implantation. Artif. Organs 29, 838-845. (doi:10.1111/j.1525-1594.2005.00137.x)
69. Patel, V. V., Zhao, L., Wong, P., Kanim, L., Bae, H. W., Pradhan, B. B. & Delamarter, R. B. 2006 Controlling bone morphogenetic protein diffusion and bone morphogenetic protein-stimulated bone growth using fibrin glue. Spine 31, 1201-1206. (doi:10.1097/01.brs.0000217650.90861.99)
70. Ryan, E. A., Mockros, L. F., Weisel, J. W. & Lorand, L. 1999 Structural origins of fibrin clot rheology. Biophys. J. 77, 2813-2826.
71. Sahni, A. & Francis, C. W. 2000 Vascular endothelial growth factor binds to fibrinogen and fibrin and stimulates endothelial cell proliferation. Blood 96, 3772-3778.
72. Sahni, A., Odrljin, T. & Francis, C. W. 1998 Binding of basic fibroblast growth factor to fibrinogen and fibrin. J. Biol. Chem. 273, 7554-7559. (doi:10.1074/jbc.273.13.7554)
73. Santoro, E., Agresta, F., Buscaglia, F., Mulieri, G., Mazzarolo, G., Bedin, N. & Mulieri, M. 2007 Preliminary experience using fibrin glue for mesh fixation in 250 patients undergoing minilaparoscopic transabdominal preperitoneal hernia repair. J. Laparoendosc. Adv. Surg. Tech. A 17, 12-15. (doi:10.1089/lap.2006.0107)
74. Schmoekel, H. G., Weber, F. E., Schense, J. C., Gratz, K. W., Schawalder, P. & Hubbell, J. A. 2005 Bone repair with a form of BMP-2 engineered for incorporation into fibrin cell ingrowth matrices. Biotechnol. Bioeng. 89, 253-262. (doi:10.1002/bit.20168)
75. Sell, S., Barnes, C., Simpson, D. & Bowlin, G. 2008 Scaffold permeability as a means to determine fiber diameter and pore size of electrospun fibrinogen. J. Biomed. Mater. Res. A 85, 115-126. (doi:10.1002/jbm.a.31556)
76. Shah, J. & Janmey, P. 1997 Strain hardening of fibrin gels and plasma clots. Rheol. Acta 36, 262-268. (doi:10.1007/s003970050044)
77. Sreerekha, P. R. & Krishnan, L. K. 2006 Cultivation of endothelial progenitor cells on fibrin matrix and layering on dacron/polytetrafluoroethylene vascular grafts. Artif. Organs 30, 242-249. (doi:10.1111/j.1525- 1594.2006.00211.x)
78. Storm, C., Pastore, J. J., MacKintosh, F. C., Lubensky, T. C. & Janmey, P. A. 2005 Nonlinear elasticity in biological gels. Nature 435, 191-194. (doi:10.1038/nature03521)
79. Taylor, S. J. & Sakiyama-Elbert, S. E. 2006 Effect of controlled delivery of neurotrophin-3 from fibrin on spinal cord injury in a long term model. J. Control. Rel. 116, 204-210. (doi:10.1016/j.jconrel.2006. 07.005)
80. Teo, W. E., He, W. & Ramakrishna, S. 2006 Electrospun scaffold tailored for tissue-specific extracellular matrix. Biotechnol. J. 1, 918-929. (doi:10.1002/biot.200600044)
81. Torio-Padron, N., Baerlecken, N., Momeni, A., Stark, G. B. & Borges, J. 2007 Engineering of adipose tissue by injection of human preadipocytes in fibrin. Aesthetic Plast. Surg. 31, 285-293. (doi:10.1007/s00266- 006-0221-6)
82. Tsai, E. C., Dalton, P. D., Shoichet, M. S. & Tator, C. H. 2006 Matrix inclusion within synthetic hydrogel guidance channels improves specific supraspinal and local axonal regeneration after complete spinal cord transection. Biomaterials 27, 519-533. (doi:10.1016/j. biomaterials.2005.07.025)
83. Wagner, O. I., Rammensee, S., Korde, N., Wen, Q., Leterrier, J. F. & Janmey, P. A. 2007 Softness, strength and selfrepair in intermediate filament networks. Exp. Cell Res. 313, 2228-2235. (doi:10.1016/j.yexcr. 2007.04.025)
84. Weisel, J. W. 2004 The mechanical properties of fibrin for basic scientists and clinicians. Biophys. Chem. 112, 267-276. (doi:10.1016/j.bpc.2004.07.029)
85. Weisel, J. W. 2005 Fibrinogen and fibrin. Adv. Protein Chem. 70, 247-299. (doi:10.1016/S0065-3233(05)70008-5)
86. Weisel, J. W. 2007a Structure of fibrin: impact on clot stability. J. Thromb. Haemost. 5(Suppl. 1), 116-124. (doi:10.1111/j.1538- 7836.2007.02504.x)
87. Weisel, J. W. 2007b Which knobs fit into which holes in fibrin polymerization. J. Thromb. Haemost. 5, 2340-2343. (doi:10.1111/j.1538-7836.2007.02794.x)
88. Weisel, J. W. & Cederholm-Williams, S. A. 1997 Fibrinogen and fibrin: characterization, processing and medical applications. In Handbook of biodegradable polymers (eds A. J. Domb, J. Kost & D. M. Wiseman), pp. 347-365. Amsterdam, The Netherlands: Harwood.
89. Weisel, J. W., Nagaswami, C. & Makowski, L. 1987 Twisting of fibrin fibers limits their radial growth. Proc. Natl Acad. Sci. USA 84, 8991-8995. (doi:10.1073/pnas.84.24.8991)
90. Willerth, S. M., Arendas, K. J., Gottlieb, D. I. & Sakiyama-Elbert, S. E. 2006 Optimization of fibrin scaffolds for differentiation of murine embryonic stem cells into neural lineage cells. Biomaterials 27, 5990-6003. (doi:10.1016/j.biomaterials.2006.07.036)
91. Willerth, S. M., Johnson, P. J., Maxwell, D. J., Parsons, S. R., Doukas, M. E. & Sakiyama-Elbert, S. E. 2007 Rationally designed peptides for controlled release of nerve growth factor from fibrin matrices. J. Biomed. Mater. Res. A 80, 13-23. (doi:10.1002/jbm.a.30844)
92. Yoshida, K. & Munakata, H. 2007 Connective tissue growth factor binds to fibronectin through the type I repeat modules and enhances the affinity of fibronectin to fibrin. Biochim. Biophys. Acta 1770, 672-680. (doi:10.1016/j.bbagen.2006.11.010)
93. Young, J. Z. & Medawar, P. B. 1940 Fibrin suture of peripheral nerves. Lancet 236, 126-132. (doi:10.1016/S0140-6736(01)07978-8)