Microstructural and mechanical differences between digested collagen-fibrin co-gels and pure collagen and fibrin gels

Acta Biomaterialia

Volumn 8, Issue 11, 2012, Pages 4031-4042

  Lai, Victor K ^a   Frey, Christina R ^a   Kerandi, Allan M ^a   Lake, Spencer P ^a   Tranquillo, Robert T ^a   Barocas, Victor H ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Collagen; Confocal microscopy; Fibrin; Mechanical properties; Microstructure; Tissue engineering

Indexed keywords

BIOMECHANICS; GELATION; GELS; MICROSTRUCTURE; SCAFFOLDS (BIOLOGY); TISSUE;

COLLAGEN GELS; COLLAGEN NETWORKS; EXTRACELLULAR MATRIX COMPONENTS; FIBRIN; FIBRIN GELS; INDIVIDUAL PROTEINS; MECHANICAL; MICRO-STRUCTURAL; PROPERTY; TISSUES ENGINEERINGS;

COLLAGEN;

COLLAGEN; COLLAGENASE; FIBRIN; PLASMIN;

ARTICLE; CO GELATION; CONFOCAL MICROSCOPY; EXTRACELLULAR MATRIX; GEL; GELATION; IMAGE RECONSTRUCTION; MORPHOLOGY; PRIORITY JOURNAL; SCANNING ELECTRON MICROSCOPY; ANIMAL; CATTLE; CHEMISTRY; MECHANICAL STRESS; MECHANICS; OSMOLARITY; PH; RAT; TENSILE STRENGTH; ULTRASTRUCTURE;

ANIMALS; CATTLE; COLLAGEN; FIBRIN; GELS; HYDROGEN-ION CONCENTRATION; MECHANICAL PHENOMENA; OSMOLAR CONCENTRATION; RATS; STRESS, MECHANICAL; TENSILE STRENGTH;

EID: 84873941685     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2012.07.010     Document Type: Article

References (52)

1. Prockop JD. Collagens: molecular biology, diseases, and potentials for therapy. Annu Rev Biochem 1995;64:403-34.
2. Cummings CL, Gawlitta D, Nerem RM, Stegemann JP. Properties of engineered vascular constructs made from collagen, fibrin, and collagen-fibrin mixtures. Biomaterials 2004;25:3699-706. (Pubitemid 38327058)
3. Buttafoco L, Kolkman NG, Engbers-Buijtenhuijs P, Poot AA, Dijkstra PJ, Vermes I, et al. Electrospinning of collagen and elastin for tissue engineering applications. Biomaterials 2006;27:724-34. (Pubitemid 41483823)
4. Grassl ED, Oegema TR, Tranquillo RT. Fibrin as an alternative biopolymer to type-I collagen for the fabrication of a media equivalent. J Biomed Mater Res 2002;60:607-12. (Pubitemid 34492599)
5. Ross J, Tranquillo R. ECM gene expression correlates with in vitro tissue growth and development in fibrin gel remodeled by neonatal smooth muscle cells. Matrix Biol 2003;22:477-90. (Pubitemid 37518307)
6. Robinson PS, Johnson SL, Evans MC, Barocas VH, Tranquillo RT. Functional tissue-engineered valves from cell-remodeled fibrin with commissural alignment of cell-produced collagen. Tissue Eng A 2008;14:83-95. (Pubitemid 351520445)
7. Syedain ZH, Weinberg JS, Tranquillo RT. Cyclic distension of fibrin-based tissue constructs: evidence of adaptation during growth of engineered connective tissue. Proc Natl Acad Sci USA 2008;105:6537-42. (Pubitemid 351754542)
8. Christiansen DL, Huang EK, Silver FH. Assembly of type I collagen: Fusion of fibril subunits and the influence of fibril diameter on mechanical properties. Matrix Biol 2000;19:409-20.
9. Diamant J, Keller A, Baer E, Litt M, Arridge RGC. Collagen; ultrastructure and its relation to mechanical properties as a function of ageing. Proc R Soc Lond Biol 1972;180:293-315.
10. Eppell SJ, Smith BN, Kahn H, Ballarini R. Nano measurements with microdevices: mechanical properties of hydrated collagen fibrils. J R Soc Interface 2006;3:117-21. (Pubitemid 46682210)
11. Liu W, Jawerth LM, Sparks EA, Falvo MR, Hantgan RR, Superfine R, et al. Fibrin fibers have extraordinary extensibility and elasticity. Science 2006;313:634. (Pubitemid 44201134)
12. Mosesson MW. Fibrinogen and fibrin structure and functions. J Thromb Haemost 2005;3:1894-904. (Pubitemid 41716577)
13. Roska FJ, Ferry JD. Studies of fibrin film. I. Stress relaxation and birefringence. Biopolymers 1982;21:1811-32. (Pubitemid 13253076)
14. Roska FJ, Ferry JD, Lin JS, Anderegg JW. Studies of fibrin film. II. Small-Angle Xray scattering. Biopolymers 1982;21:1833-45. (Pubitemid 13253077)
15. Pezzin G, Scandola M, Gotte L. The low temperature mechanical relaxation of elastin. I. The dry protein. Biopolymers 1976;15:283-92.
16. Scandola M, Pezzin G. The low temperature mechanical relaxation of elastin. II. The solvated protein. Biopolymers 1978;17:213-23. (Pubitemid 8275368)
17. Yonese M, Baba K, Kishimoto H. Viscoelastic properties of poly(vinyl alcohol)/alginate snake-cage hydrogels and interpenetrating hydrogels. Polym J 1992;24:395-404.
18. Mathew AP, Packirisamy S, Thomas S. Morphology, mechanical properties, and failure topography of semi-interpenetrating polymer networks based on natural rubber and polystyrene. J Appl Polym Sci 2000;78:2327-44. (Pubitemid 32027543)
19. Santin M, Huang SJ, Iannace S, Ambrosio L, Nicolais L, Peluso G. Synthesis and characterization of a new interpenetrated poly(2- hydroxyethylmethacrylate)-gelatin composite polymer. Biomaterials 1996;17:1459-67. (Pubitemid 26254174)
20. Lai VK, Lake SP, Frey CR, Tranquillo RT, Barocas VH. Mechanical behavior of collagen-fibrin co-gels reflects transition from series to parallel interactions with increasing collagen content. J Biomech Eng 2012;134:011004.
21. Rowe SL, Stegemann JP. Interpenetrating collagen-fibrin composite matrices with varying protein contents and ratios. Biomacromolecules 2006;7:2942-8. (Pubitemid 46039946)
22. Mosher DF, Schad PE. Cross-linking of fibronectin to collagen by blood coagulation factor XIIIa. J Clin Invest 1979;64:781-7. (Pubitemid 10223757)
23. Stemberger A, Jilek F, Hormann H, Blumel G. Fibrinogen-1collagen interactions. Thromb Haemost 1977;38:305.
24. Duckert F, Nyman D. Factor XIII. Fibrin and collagen. Suppl Thromb Haemost 1978;63:391-6.
25. Ferry JD, Morrison PR. Preparation and properties of serum and plasma proteins. VIII. The conversion of human fibrinogen to fibrin under various conditions. J Am Chem Soc 1947;69:388-400.
26. Blombäck B, Carlsson K, Fatah K, Hessel B, Procyk R. Fibrin in human plasma: gel architectures governed by rate and nature of fibrinogen activation. Thromb Res 1994;75:521-38. (Pubitemid 24267336)
27. Blombäck B, Carlsson K, Hessel B, Liljeborg A, Procyk R, Åslund N. Native fibrin gel networks observed by 3D microscopy, permeation and turbidity. Biochim Biophys Acta Protein Struct Mol Enzymol 1989;997:96-110. (Pubitemid 19178601)
28. Akpalo E, Larreta-Garde V. Increase of fibrin gel elasticity by enzymes: A kinetic approach. Acta Biomater 2010;6:396-402.
29. Shen LL, McDonagh RP, McDonagh J, Hermans J. Fibrin gel structure: Influence of calcium and covalent cross-linking on the elasticity. Biochem Biophys Res Commun 1974;56:793-8.
30. Kaibara M, Fukada E. Effect of temperature on dynamic viscoelasticity during the clotting reaction of fibrin. Biochim Biophys Acta Gen Subj 1977;499:352-61. (Pubitemid 8207799)
31. Dubey N, Letourneau PC, Tranquillo RT. Neuronal contact guidance in magnetically aligned fibrin gels: effect of variation in gel mechano-structural properties. Biomaterials 2001;22:1065-75. (Pubitemid 32229932)
32. Rowe SL, Lee SY, Stegemann JP. Influence of thrombin concentration on the mechanical and morphological properties of cell-seeded fibrin hydrogels. Acta Biomater 2007;3:59-67. (Pubitemid 44804296)
33. Naito M, Nomura H, Iguchi A, Thompson WD, Smith EB. Effect of crosslinking by factor XIIIa on the migration of vascular smooth muscle cells into fibrin gels. Thromb Res 1998;90:111-6. (Pubitemid 28343527)
34. Mol A, van Lieshout MI, Dam-de Veen CG, Neuenschwander S, Hoerstrup SP, Baaijens FPT, et al. Fibrin as a cell carrier in cardiovascular tissue engineering applications. Biomaterials 2005;26:3113-21. (Pubitemid 39647246)
35. Ho W, Tawil B, Dunn JCY, Wu BM. The behavior of human mesenchymal stem cells in 3D fibrin clots: dependence on fibrinogen concentration and clot structure. Tissue Eng 2006;12:1587-95. (Pubitemid 44174792)
36. Wood GC, Keech MK. The formation of fibrils from collagen solutions 1. The effect of experimental conditions: kinetic and electron-microscope studies. Biochem J 1960;75:588-98.
37. Roeder BA, Kokini K, Sturgis JE, Robinson JP, Voytik-Harbin SL. Tensile mechanical properties of three-dimensional type I collagen extracellular matrices with varied microstructure. J Biomech Eng 2002;124:214-22. (Pubitemid 34407065)
38. Mosesson MW, Siebenlist KR, Meh DA. The structure and biological features of fibrinogen and fibrin. Ann NY Acad Sci 2001;936:11-30. (Pubitemid 32613890)
39. Kadler KE, Holmes DF, Trotter JA, Chapman JA. Collagen fibril formation. Biochem J 1996;316:1-11. (Pubitemid 26158194)
40. Eb S. Fibrinogen, fibrin and fibrin degradation products in relation to atherosclerosis. Clin Haematol 1986;15:355.
41. Martin P. Wound healing-Aiming for perfect skin regeneration. Science 1997;276:75-81. (Pubitemid 27161246)
42. Stein AM, Vader DA, Jawerth LM, Weitz DA, Sander LM. An algorithm for extracting the network geometry of three-dimensional collagen gels. J Microsc 2008;232:463-75.
43. Lewis JL, Johnson SL, Oegema TR. Interfibrillar collagen bonding exists in matrix produced by chondrocytes in culture: evidence by electron microscopy. Tissue Eng 2002;8:989-95. (Pubitemid 35397244)
44. Fratzl P, Misof K, Zizak I, Rapp G, Amenitsch H, Bernstorff S. Fibrillar structure and mechanical properties of collagen. J Struct Biol 1998;122:119-22. (Pubitemid 28411191)
45. Chandran PL, Barocas VH. Microstructural mechanics of collagen gels in confined compression: poroelasticity, viscoelasticity, and collapse. J Biomech Eng 2004;126:152-66. (Pubitemid 38621128)
46. Tower TT, Neidert MR, Tranquillo RT. Fiber alignment imaging during mechanical testing of soft tissues. Ann Biomed Eng 2002;30:1221-33.
47. Stuart K, Panitch A. Influence of chondroitin sulfate on collagen gel structure and mechanical properties at physiologically relevant levels. Biopolymers 2008;89:841-51.
48. Purohit PK, Litvinov RI, Brown AEX, Discher DE, Weisel JW. Protein unfolding accounts for the unusual mechanical behavior of fibrin networks. Acta Biomater 2011;7:2374-83.
49. Soulhat J, Buschmann MD, Shirazi-Adl A. A fibril-network-reinforced biphasic model of cartilage in unconfined compression. J Biomech Eng 1999;121: 340-7. (Pubitemid 29318310)
50. Nachtrab S, Kapfer SC, Arns CH, Madadi M, Mecke K, Schröder-Turk GE. Morphology and linear-elastic moduli of random network solids. Adv Mater 2011;23:2633-7.
51. Stylianopoulos T, Barocas VH. Volume-Averaging theory for the study of the mechanics of collagen networks. Comput Methods Appl Mech Eng 2007;196: 2981-90. (Pubitemid 46722279)
52. Sander EA, Stylianopoulos T, Tranquillo RT, Barocas VH. Image-based multiscale modeling predicts tissue-level and network-level fiber reorganization in stretched cell-compacted collagen gels. Proc Natl Acad Sci USA 2009;106:17675-80.