Modeling of fibroblast-controlled strengthening and remodeling of uniaxially constrained collagen gels

Journal of Biomechanical Engineering

Volumn 132, Issue 11, 2010, Pages

  Kroon, Martin ^a  

^a ROYAL INSTITUTE OF TECHNOLOGY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN FIBER; COLLAGEN FIBRILS; COLLAGEN GELS; FORCE-STRAIN CURVES; MATERIAL STIFFNESS; THEORETICAL MODELS;

CELL CULTURE; FIBERS; FIBROBLASTS; STRENGTHENING (METAL); TISSUE;

COLLAGEN;

COLLAGEN FIBER; COLLAGEN FIBRIL; COLLAGEN GEL; COLLAGEN;

ARTICLE; FIBROBLAST; PREDICTION; RIGIDITY; THEORY; BIOLOGICAL MODEL; BIOMECHANICS; CHEMISTRY; GEL; HUMAN; IN VITRO STUDY; MECHANICAL STRESS; PHYSIOLOGY; TENSILE STRENGTH;

BIOMECHANICS; COLLAGEN; FIBROBLASTS; GELS; HUMANS; MODELS, BIOLOGICAL; STRESS, MECHANICAL; TENSILE STRENGTH;

EID: 77958586627     PISSN: 01480731     EISSN: 15288951     Source Type: Journal    
DOI: 10.1115/1.4002666     Document Type: Article

References (59)

1. Majamaa K. Savolainen E.R. Myllylä V.V. Synthesis of Structurally Unstable Type III Procollagen in Patients With Cerebral Artery Aneurysm. Biochim. Biophys. Acta 1992, 1138:191-196. BBACAQ, 0006-3002.
2. Austin G. Fisher S. Dickson D. Anderson D. Richardson S. The Significance of the Extracellular Matrix in Intracranial Aneurysms. Ann. Clin. Lab. Sci. 1993, 23:97-105. ACLSCP, 0091-7370.
3. Barnes M.J. Collagens in Atherosclerosis. Coll. Relat. Res. 1985, 5:65-97. 0174-173X.
4. Bishop J.E. Lindahl G. Regulation of Cardiovascular Collagen Synthesis by Mechanical Load. Cardiovasc. Res. 1999, 42:27-44. CVREAU, 0008-6363, 10.1016/S0008-6363(99)00021-8.
5. Canham P.B. Finlay H.M. Dixon J.G. Ferguson S.E. Layered Collagen Fabric of Cerebral Aneurysms Quantitatively Assessed by the Universal Stage and Polarized Light Microscopy. Anat. Rec. 1991, 231:579-592. ANREAK, 0003-276X, 10.1002/ar.1092310420.
6. Dallon J.C. Sherratt J.A. A Mathematical Model for Fibroblast and Collagen Orientation. Bull. Math. Biol. 1998, 60:101-129. BMTBAP, 0092-8240, 10.1006/bulm.1997.0027.
7. Merrilees M.J. Tiang K.M. Scott L. Changes in Collagen Fibril Diameters Across Artery Walls Including a Correlation With Glycosaminoglycan Content. Connect. Tissue Res. 1987, 16:237-257. CVTRBC, 0300-8207, 10.3109/03008208709006979.
8. Fung Y.C. Biomechanics. Mechanical Properties of Living Tissues 1993, 2nd ed., Springer-Verlag, New York.
9. Cukierman E. Pankov R. Stevens D.R. Yamada K.M. Taking Cell-Matrix Adhesions to the Third Dimension. Science 2001, 294:1708-1712. SCIEAS, 0036-8075, 10.1126/science.1064829.
10. Jiang H. Grinnell F. Cell-Matrix Entanglement and Mechanical Anchorage of Fibroblasts in Three-Dimensional Collagen Matrices. Mol. Biol. Cell 2005, 16:5070-5076. MBCEEV, 1059-1524, 10.1091/mbc.E05-01-0007.
11. Barocas V.H. Moon A.G. Tranquillo R.T. The Fibroblast-Populated Collagen Microsphere Assay of Cell Traction Force-Part 2: Measurement of the Cell Traction Parameter. ASME J. Biomech. Eng. 1995, 117:161-170. JBENDY, 0148-0731, 10.1115/1.2795998.
12. Dembo M. Wang Y.-.L. Stresses at the Cell-to-Substrate Interface During Locomotion of Fibroblasts. Biophys. J. 1999, 76:2307-2316. BIOJAU, 0006-3495, 10.1016/S0006-3495(99)77386-8.
13. Eastwood M. McGrouther D.A. Brown R.A. Fibroblast Responses to Mechanical Forces. Proc. Inst. Mech. Eng., Part H: J. Eng. Med. 1998, 212:85-92. PIHMEQ, 0954-4119, 10.1243/0954411981533854.
14. Engler A. Bacakova L. Newman C. Hategan A. Griffin M. Discher D. Substrate Compliance Versus Ligand Density in Cell on Gel Responses. Biophys. J. 2004, 86:617-628. BIOJAU, 0006-3495, 10.1016/S0006-3495(04)74140-5.
15. Friedl P. Bröcker E.-.B. The Biology of Cell Locomotion Within Three-Dimensional Extracellular Matrix. Cell. Mol. Life Sci. 2000, 57:41-64. CMLSFI, 1420-682X, 10.1007/s000180050498.
16. Friedrichs J. Taubenberger A. Franz C.M. Muller D.J. Cellular Remodeling of Individual Collagen Fibrils Visualized by Time-Lapse AFM. J. Mol. Biol. 2007, 372:594-607. JMOBAK, 0022-2836, 10.1016/j.jmb.2007.06.078.
17. Grinnell F. Fibroblast Biology in Three-Dimensional Collagen Matrices. Trends Cell Biol. 2003, 13:264-269. TCBIEK, 0962-8924, 10.1016/S0962-8924(03)00057-6.
18. Lo C.-.M. Wang H.-.B. Dembo M. Wang Y. Cell Movement Is Guided by the Rigidity of the Substrate. Biophys. J. 2000, 79:144-152. BIOJAU, 0006-3495, 10.1016/S0006-3495(00)76279-5.
19. Poole K. Khairy K. Friedrichs J. Franz C. Cisneros D.A. Howard J. Mueller D. Molecular-Scale Topographic Cues Induce the Orientation and Directional Movement of Fibroblasts on Two-Dimensional Collagen Surfaces. J. Mol. Biol. 2005, 349:380-386. JMOBAK, 0022-2836, 10.1016/j.jmb.2005.03.064.
20. Birk D.E. Zycband E.I. Winkelmann D.A. Trelstad R.L. Collagen Fibrillogenesis In Situ. Discontinuous Segmental Assembly in Extracellular Compartments. Ann. N.Y. Acad. Sci. 1990, 580:176-194. ANYAA9, 0077-8923, 10.1111/j.1749-6632.1990.tb17928.x.
21. Cisneros D.A. Hung C. Franz C.M. Muller D.J. Observing Growth Steps of Collagen Self-Assembly by Time-Lapse High-Resolution Atomic Force Microscopy. J. Struct. Biol. 2006, 154:232-245. JSBIEM, 1047-8477, 10.1016/j.jsb.2006.02.006.
22. Huang D. Chang T.R. Aggarwal A. Lee R.C. Ehrlich H.P. Mechanisms and Dynamics of Mechanical Strengthening in Ligament-Equivalent Fibroblast-Populated Collagen Matrices. Ann. Biomed. Eng. 1993, 21:289-305. ABMECF, 0090-6964, 10.1007/BF02368184.
23. Lin H. Clegg D.O. Lal R. Imaging Real-Time Proteolysis of Single Collagen I Molecules With an Atomic Force Microscope. Biochemistry 1999, 38:9956-9963. BICHAW, 0006-2960, 10.1021/bi990800q.
24. Meshel A.S. Wei Q. Adelstein R.S. Sheetz M.P. Basic Mechanism of Three-Dimensional Collagen Fibre Transport by Fibroblasts. Nat. Cell Biol. 2005, 7:157-164. NCBIFN, 1465-7392, 10.1038/ncb1216.
25. Tóth M. Násady G.L. Nyáry I. Kerényi T. Orosz M. Molnárka G. Monos E. Sterically Inhomogenous Viscoelastic Behavior of Human Saccular Cerebral Aneurysms. J. Vasc. Res. 1998, 35:345-355. JVREE9, 1018-1172, 10.1159/000025604.
26. Pelham R.J. Wang Y. Cell Locomotion and Focal Adhesions Are Regulated by Substrate Flexibility. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:13661-13665. PNASA6, 0027-8424, 10.1073/pnas.94.25.13661.
27. Weyts F.A. A. Bosmans B. Niesing R. Leeuwen J.P. T. M. Weinans H. Mechanical Control of Human Osteoblast Apoptosis and Proliferation in Relation to Differentiation. Calcif. Tissue Int. 2003, 72:505-512. CTINDZ, 0171-967X, 10.1007/s00223-002-2027-0.
28. Pedersen J.A. Swartz M.A. Mechanobiology in the Third Dimension. Ann. Biomed. Eng. 2005, 33:1469-1490. ABMECF, 0090-6964, 10.1007/s10439-005-8159-4.
29. Barocas V.H. Tranquillo R.T. An Anisotropic Biphasic Theory of Tissue-Equivalent Mechanics: The Interplay Among Cell Traction, Fibrillar Network Deformation, Fibril Alignment, and Cell Contact Guidance. ASME J. Biomech. Eng. 1997, 119:137-145. JBENDY, 0148-0731, 10.1115/1.2796072.
30. Chandran P.L. Barocas V.H. Affine Versus Non-Affine Fibril Kinematics in Collagen Networks: Theoretical Studies of Network Behavior. ASME J. Biomech. Eng. 2006, 128:259-270. JBENDY, 0148-0731, 10.1115/1.2165699.
31. Driessen N.J. B. Peters G.W. M. Huyghe J.M. Bouten C.V. C. Baaijens F.P. T. Remodelling of Continuously Distributed Collagen Fibres in Soft Connective Tissues. J. Biomech. 2003, 36:1151-1158. JBMCB5, 0021-9290, 10.1016/S0021-9290(03)00082-4.
32. Farquhar T. Dawson P.R. Torzilli P.A. A Microstructural Model for the Anisotropic Drained Stiffness of Articular Cartilage. ASME J. Biomech. Eng. 1990, 112:414-425. JBENDY, 0148-0731, 10.1115/1.2891205.
33. Lanir Y. Rheological Behavior of the Skin-Experimental Results and a Structural Model. Biorheology 1979, 16:191-202. BRHLAU, 0006-355X.
34. Soulhat J. Buschmann M.D. Shirazi-Adl A. A Fibril-Network-Reinforced Biphasic Model of Cartilage in Unconfined Compression. ASME J. Biomech. Eng. 1999, 121:340-347. JBENDY, 0148-0731, 10.1115/1.2798330.
35. Baek S. Rajagopal K.R. Humphrey J.D. A Theoretical Model of Enlarging Intracranial Fusiform Aneurysms. ASME J. Biomech. Eng. 2006, 128:142-149. JBENDY, 0148-0731, 10.1115/1.2132374.
36. Driessen N.J. B. Wilson W. Bouten C.V. C. Baaijens F.P. T. A Computational Model for Collagen Fibre Remodelling in the Arterial Wall. J. Theor. Biol. 2004, 226:53-64. JTBIAP, 0022-5193, 10.1016/j.jtbi.2003.08.004.
37. Humphrey J.D. Remodeling of a Collagenous Tissue at Fixed Lengths. ASME J. Biomech. Eng. 1999, 121:591-597. JBENDY, 0148-0731, 10.1115/1.2800858.
38. Humphrey J.D. Rajagopal K.R. A Constrained Mixture Model for Growth and Remodeling of Soft Tissues. Math. Models Meth. Appl. Sci. 2002, 12:407-430. MMMSEU, 0218-2025, 10.1142/S0218202502001714.
39. Kroon M. Holzapfel G.A. A Model for Saccular Cerebral Aneurysm Growth by Collagen Fibre Remodelling. J. Theor. Biol. 2007, 247:775-787. JTBIAP, 0022-5193, 10.1016/j.jtbi.2007.03.009.
40. Kroon M. Holzapfel G.A. Modelling of Saccular Aneurysm Growth in a Human Middle Cerebral Artery. ASME J. Biomech. Eng. 2008, 130:051012. JBENDY, 0148-0731, 10.1115/1.2965597.
41. Kroon M. Holzapfel G.A. A Theoretical Model for Fibroblast-Controlled Growth of Saccular Cerebral Aneurysms. J. Theor. Biol. 2009, 257:73-83. JTBIAP, 0022-5193, 10.1016/j.jtbi.2008.10.021.
42. Rachev A. Stergiopulos N. Meister J.-.J. Theoretical Study of Dynamics of Arterial Wall Remodeling in Response to Changes in Blood Pressure. J. Biomech. 1996, 29:635-642. JBMCB5, 0021-9290, 10.1016/0021-9290(95)00108-5.
43. Ryan J.M. Humphrey J.D. Finite Element Based Predictions of Preferred Material Symmetries in Saccular Aneurysms. Ann. Biomed. Eng. 1999, 27:641-647. ABMECF, 0090-6964, 10.1114/1.208.
44. Taber L.A. Humphrey J.D. Stress-Modulated Growth, Residual Stress, and Vascular Heterogeneity. ASME J. Biomech. Eng. 2001, 123:528-535. JBENDY, 0148-0731, 10.1115/1.1412451.
45. Watton P.N. Hill N.A. Heil M. A Mathematical Model for the Growth of the Abdominal Aortic Aneurysm. Biomech. Model. Mechanobiol. 2004, 3:98-113. BMMICD, 1617-7959, 10.1007/s10237-004-0052-9.
46. Rodriguez E.K. Hoger A. McCulloch A.D. Stress-Dependent Finite Growth in Soft Elastic Tissues. J. Biomech. 1994, 27:455-467. JBMCB5, 0021-9290, 10.1016/0021-9290(94)90021-3.
47. Diamant J. Keller A. Baer E. Litt M. Arridge R.G. C. Collagen; Ultrastructure and Its Relation to Mechanical Properties as a Function of Ageing. Proc. R. Soc. London, Ser. B 1972, 180:293-315. PRLBA4, 0962-8452, 10.1098/rspb.1972.0019.
48. Buckley C.P. Lloyd D.W. Konopasek M. On the Deformation of Slender Filaments With Planar Crimp: Theory, Numerical Solution and Applications to Tendon Collagen and Textile Materials. Proc. R. Soc. London, Ser. A 1980, 372:33-64. PRLAAZ, 0950-1207, 10.1098/rspa.1980.0101.
49. Comninou M. Yannas I.V. Dependence of Stress-Strain Nonlinearity of Connective Tissues on the Geometry of Collagen Fibers. J. Biomech. 1976, 9:427-433. JBMCB5, 0021-9290, 10.1016/0021-9290(76)90084-1.
50. Hurschler C. Loitz-Ramage B. Vanderby Jr. R. A Structurally Based Stress-Stretch Relationship for Tendon and Ligament. ASME J. Biomech. Eng. 1997, 119:392-399. JBENDY, 0148-0731, 10.1115/1.2798284.
51. Lanir Y. Structure-Function Relations in Mammalian Tendon: The Effect of Geometrical Nonuniformity. J. Bioeng. 1978, 2:119-128. 0145-3068.
52. Lanir Y. A Structural Theory for the Homogeneous Biaxial Stress-Strain Relationships in Flat Collagenous Tissues. J. Biomech. 1979, 12:423-436. JBMCB5, 0021-9290, 10.1016/0021-9290(79)90027-7.
53. Annovazzi L. Genna F. An Engineering, Multiscale Constitutive Model for Fiber-Forming Collagen in Tension. J. Biomed. Mater. Res. Part A 2010, 92:254-266. 1549-3296, 10.1002/jbm.a.32352.
54. Fung Y.C. Elasticity of Soft Tissues in Simple Elongation. Am. J. Physiol. 1967, 213:1532-1544. AJPHAP, 0002-9513.
55. Balestrini J.L. Billiar K.L. Magnitude and Duration of Stretch Modulate Fibroblast Remodeling. ASME J. Biomech. Eng. 2009, 131:051005. JBENDY, 0148-0731, 10.1115/1.3049527.
56. Kessler D. Dethlefsen S. Haase I. Plomann M. Hirche F. Krieg R. Eckes B. Fibroblasts in Mechanically Stressed Collagen Lattices Assume a 'Synthetic' Phenotype. J. Biol. Chem. 2001, 276:36575-36585. JBCHA3, 0021-9258, 10.1074/jbc.M101602200.
57. Thomopoulos S. Fomovsky G.M. Holmes J.W. The Development of Structural and Mechanical Anisotropy in Fibroblast Populated Collagen Gels. ASME J. Biomech. Eng. 2005, 127:742-750. JBENDY, 0148-0731, 10.1115/1.1992525.
58. Thomopoulos S. Fomovsky G.M. Chandran P.L. Holmes J.W. Collagen Fiber Alignment Does Not Explain Mechanical Anisotropy in Fibroblast Populated Collagen Gels. ASME J. Biomech. Eng. 2007, 129:642-650. JBENDY, 0148-0731, 10.1115/1.2768104.
59. Humphrey J.D. Wells P.B. Baek S. Hu J.-.J. McLeroy K. Yeh A.T. A Theoretically-Motivated Biaxial Tissue Culture System With Intravital Microscopy. Biomech. Model. Mechanobiol. 2008, 7:323-334. BMMICD, 1617-7959, 10.1007/s10237-007-0099-5.