A two-compartment mechanochemical model of the roles of transforming growth factor β and tissue tension in dermal wound healing

Journal of Theoretical Biology

Volumn 272, Issue 1, 2011, Pages 145-159

  Murphy, Kelly E ^a   Hall, Cameron L ^b   McCue, Scott W ^a   Sean McElwain, D L ^a  

^a QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Biomechanics; Morphoelasticity; Myofibroblasts; Zero stress states

Indexed keywords

TRANSFORMING GROWTH FACTOR BETA;

APOPTOSIS; BIOMECHANICS; CELL ORGANELLE; NUMERICAL MODEL; RESIDUAL STRESS; STRAIN; WOUNDING;

APOPTOSIS; ARTICLE; BIOMECHANICS; CELL DENSITY; CELL DIFFERENTIATION; CONTRACTURE; CONTROLLED STUDY; FIBROBLAST; MATHEMATICAL MODEL; MECHANICAL STRESS; MYOFIBROBLAST; PREDICTION; PRIORITY JOURNAL; STRESS STRAIN RELATIONSHIP; TENSION; WOUND HEALING;

EID: 78650657100     PISSN: 00225193     EISSN: 10958541     Source Type: Journal    
DOI: 10.1016/j.jtbi.2010.12.011     Document Type: Article

References (86)

1. Aarabi S., Bhatt K.A., Shi Y., Paterno J., Chang E.I., Loh S.A., Holmes J.W., Longaker M.T., Yee H., Gurtner G.C. Mechanical load initiates hypertrophic scar formation through decreased cellular apoptosis. Journal of the Federation of American Societies for Experimental Biology 2007, 21:3250-3261.
2. Ahlfors J.-E.W., Billiar K.L. Biomechanical and biochemical characteristics of a human fibroblast-produced and remodeled matrix. Biomaterials 2007, 28:2183-2191.
3. Alberts B., Bray D., Lewis J., Raff M., Roberts K., Watson J.D. The Molecular Biology of the Cell 1989, Garland Publ. Inc, New York.
4. Aumailley M., Krieg T., Razaka G., Müller P.K., Bricaud H. Influence of cell density on collagen biosynthesis in fibroblast cultures. Biochemical Journal 1982, 206:505-510.
5. Billingham R.E., Medawar P.B. Contracture and intussusceptive growth in the healing of extensive wounds in mammalian skin. Journal of Anatomy 1955, 89:114-123.
6. Billingham R.E., Russell P.S. Studies on wound healing, with special reference to the phenomenon of contracture in experimental wounds in rabbits' skin. Annals of Surgery 1956, 144:961-981.
7. Campbell, B.H., 2002. An in vitro study of human fibroblast contractility and the differential effect of tgf-β1 and tgf-β3 on fibroblast contraction and collagen synthesis. Master's Thesis, University of Pittsburgh.
8. Chapuis J.E., Agache P. A new technique to study the mechanical properties of collagen lattices. Journal of Biomechanics 1992, 25:115-117.
9. Cook, J., 1995. A mathematical model for dermal wound healing: wound contraction and scar formation. Ph.D. Thesis, University of Washington.
10. Delvoye P., Wiliquet P., Levĉque J.-L., Nusgens B.V., Lapière C.M. Measurement of mechanical forces generated by skin fibroblasts embedded in a three-dimensional collagen gel. Journal of Investigative Dermatology 1991, 97:898-902.
11. Desmouliere A., Geinoz A., Gabbiani F., Gabbiani G. Transforming growth factor-β1 induces α-smooth muscle actin expression in granulation tissue myofibroblasts and in quiescent and growing cultured fibroblasts. The Journal of Cell Biology 1993, 122:103-111.
12. Diridollou S., Black D., Lagarde J.M., Gall Y. Sex- and site-dependent variations in the thickness and mechanical properties of human skin in vivo. International Journal of Cosmetic Science 2000, 22:421-435.
13. Doillon C.J., Hembry R.M., Ehrlich H.P., Burke J.F. Actin filaments in normal dermis and during wound healing. American Journal of Pathology 1987, 126:164-170.
14. Eastwood M., McGrouther D.A., Brown R.A. A culture force monitor for measurement of contraction forces generated in human dermal fibroblast cultures: evidence for cell-matrix mechanical signalling. Biochimica et Biophysica Acta (BBA)-General Subjects 1994, 1201:186-192.
15. Eastwood M., Porter R., Khan U., McGrouther G., Brown R. Quantitative analysis of collagen gel contractile forces generated by dermal fibroblasts and the relationship to cell morphology. Journal of Cellular Physiology 1996, 166:33-42.
16. Eastwood M., McGrouther D.A., Brown R.A. Fibroblast responses to mechanical forces. Proceedings of the Institution of Mechanical Engineers. Part H: Journal of Engineering in Medicine 1998, 212:85-92.
17. Eckes B., Nischt R., Krieg T. Cell-matrix interactions in dermal repair and scarring. Fibrogenesis and Tissue Repair 2010, 3.
18. Enoch S., Leaper D.J. Basic science of wound healing. Surgery 2007, 26:31-37.
19. Enoch S., Grey J.E., Harding K.G. Abc of wound healing: recent advances and emerging treatments. British Medical Journal 2006, 332:962-965.
20. Farahani R.M., Kloth L.C. The hypothesis of 'biophysical matrix contraction': wound contraction revisited. International Wound Journal 2008, 5:477-482.
21. Ferguson M.W.J., O'Kane S. Scar-free healing: from embryonic mechanisms to adult therapeutic intervention. Philosophical Transactions of the Royal Society of London B 2004, 359:839-850.
22. Ferrenq I., Tranqui L., Vaihé B., Gumery P.Y., Tracqui P. Modelling biological gel contraction by cells: mechanocellular formulation and cell traction force quantification. Acta Biotheretica 1997, 45:267-293.
23. Fray T.R., Molloy J.E., Armitage M.O., Sparrow J.C. Quantification of single human dermal fibroblast contraction. Tissue Engineering 1998, 4:281-291.
24. Freyman T.M., Yannas I.V., Yokoo R., Gibson L.J. Fibroblast contraction of a collagen-gag matrix. Biomaterials 2001, 22:2883-2891.
25. Freyman T.M., Yannas I.V., Yokoo R., Gibson L.J. Fibroblast contractile force is independent of the stiffness which resists the contraction. Experimental Cell Research 2002, 272:153-162.
26. Gabbiani G. The myofibroblast in wound healing and fibrocontractive diseases. The Journal of Pathology 2003, 200:500-503.
27. Genzer, J., Groenewold, J., 2006. Soft matter with hard skin: From skin wrinkles to templating and material characterization. Soft Matter 2, 310-323.
28. Ghosh K., Pan Z., Guan E., Ge S., Liu Y., Nakamura T., Ren Z.-D., Rafailovich M., Clark R.A.F. Cell adaptation to a physiologically relevant ecm mimic with different viscoelastic properties. Biomaterials 2007, 28:671-679.
29. Goriely A., Ben Amar M. On the definition and modeling of incremental, cumulative, and continuous growth laws in morphelasticity. Biomechanical Models of Mechanobiology 2007, 6:289-296.
30. Grillo H.C., Watts G.T., Gross J. Studies in wound healing: I. Contraction and the wound contents. Annals of Surgery 1958, 148:145-152.
31. Grinnell F., Ho C.-H., Tamariz E., Lee D.J., Skuta G. Dendritic fibroblasts in three-dimensional collagen matrices. Molecular Biology of the Cell 2003, 14:384-395.
32. Hall, C.L., 2009. Modelling of some biological materials using continuum mechanics. Ph.D. Thesis, Queensland University of Technology.
33. Harley B.A., Freyman T.M., Wong M.Q., Gibson L.J. A new technique for calculating individual dermal fibroblast contractile forces generated within collagen-gag scaffolds. Biophysical Journal 2007, 93:2911-2922.
34. Hinz B. Formation and function of the myofibroblast during tissue repair. Journal of Investigative Dermatology 2007, 127:526-537.
35. Hinz B. Tissue stiffness, latent tgf-β1 activation, and mechanical signal transduction: implications for the pathogenesis and treatment of fibrosis. Journal Current Rheumatology Reports 2009, 11:120-126.
36. Hinz B. The myofibroblast: paradigm for a mechanically active cell. Journal of Biomechanics 2010, 43:146-155.
37. Hinz B., Gabbiani G. Mechanisms of force generation and transmission by myofibroblasts. Current Opinion in Biotechnology 2003, 14:538-546.
38. Hinz B., Mastrangelo D., Iselin C.E., Chaponnier C., Gabbiani G. Mechanical tension controls granulation tissue contractile activity and myofibroblast differentiation. American Journal of Pathology 2001, 159:1009-1020.
39. Javierre E., Moreo P., Doblaré M., García-Aznar J.M. Numerical modeling of a mechano-chemical theory for wound contraction analysis. International Journal of Solids and Structures 2009, 46:3597-3606.
40. Kennedy D.F., Cliff W.J. A systematic study of wound contraction in mammalian skin. Pathology 1979, 11:207-222.
41. Khatyr F., Imberdis C., Vescovo P., Varchon D., Lagarde J.-M. Model of the viscoelastic behaviour of skin in vivo and the study of anisotropy. Skin Research and Technology 2004, 10:96-103.
42. Khorramizadeh M.R., Tredget E.E., Telasky C., Shen Q., Ghahary A. Aging differentially modulates the expression of collagen and collagenase in dermal fibroblasts. Molecular and Cellular Biochemistry 1999, 194:99-108.
43. Kim Y., Friedman A. Interaction of tumor with its micro-environment: a mathematical model. Bulletin of Mathematical Biology 2009, 72:1029-1068.
44. Kolodney M.S., Wysolmerski R.B. Isometric contraction by fibroblasts and endothelial cells in tissue culture: a quantitative study. The Journal of Cell Biology 1992, 117:73-82.
45. Kucharova M., Ďoubal S., Lemera P., Rejchrt P., Navrátil M. Viscoelasticity of biological materials-measurement and practical impact on biomedicine. Physiological Research 2007, 56(Suppl. 1):S33-S37.
46. Li, B., Wang, J.H.-C., Fibroblasts and myofibroblasts in wound healing: force generation and measurement. Journal of Tissue Viability, doi:, in press. http://10.1016/j.jtv.2009.11.004.
47. Luccioli G.M., Kahn D.S., Robertson H.R. Histologic study of wound contraction in the rabbit. Annals of Surgery 1964, 160:1030-1040.
48. Majno G., Joris I. Cells, Tissues and Diseases-Principles of General Pathology 2004, Oxford University Press. second ed.
49. Masur S.K., Dewal H.S., Dinh T.T., Erenburg I., Petridou S. Myofibroblasts differentiate from fibroblasts when plated at low density. Proceedings of the National Academy of Sciences of the United States of America 1996, 93:4219-4223.
50. McGrath M.H., Emery J.M. The effect of inhibition of angiogenesis in granulation tissue on wound healing and the fibroblast. Annals of Plastic Surgery 1985, 15:105-122.
51. McGrath M.H., Simon R.H. Wound geometry and the kinetics of wound contraction. Plastic and Reconstructive Surgery 1983, 72:66-72.
52. Morgan, C.J., Pledger, W.J., 1992. Wound healing: biochemical and clinical aspects, Saunders, Philadelphia, London, pp. 63-76 (Chapter 4).
53. Moulin V., Castilloux G., Jean A., Garrel D.R., Auger F.A., Germain L. In vitro models to study wound healing fibroblasts. Burns 1996, 22:359-362.
54. Moulin V., Castilloux G., Auger F.A., Garrel D.R., O'Connor-McCourt M.D., Germain L. Modulated response to cytokines of human wound healing myofibroblasts compared to dermal fibroblasts. Experimental Cell Research 1998, 238:283-293.
55. Moulin V., Larochelle S., Langlois C., Thibault I., Lopez-Vallé C.A., Roy M. Normal skin wound and hypertrophic scar myofibroblasts have differential responses to apoptotic inductors. Journal of Cellular Physiology 2004, 198:350-358.
56. Murata H., Zhou L., Ochoa S., Hasan A., Badiavas E., Falanga V. Tgf-β3 stimulates and regulates collagen synthesis through tgf β1-dependent and independent mechanisms. Journal of Investigative Dermatology 1997, 108:258-262.
57. Murray, J.D., 2003. Mathematical Biology II: Spatial Models and Biomedical Applications. Interdisciplinary Applied Mathematics, vol. 18, three ed. Springer.
58. Olsen L., Sherratt J.A., Maini P.K. A mechanochemical model for adult dermal wound contraction and the permanence of the contracted tissue displacement profile. Journal of Theoretical Biology 1995, 17:113-128.
59. Olsen L., Sherratt J.A., Maini P.K. A mathematical model for fibro-proliferative wound healing disorders. Bulletin of Mathematical Biology 1996, 58:787-808.
60. Olsen L., Sherratt J.A., Maini P.K. A mechanochemical model for normal and abnormal dermal wound repair. Nonlinear Analysis 1997, 30:3333-3338.
61. Olsen L., Sherratt J.A., Maini P.K. Spatially varying equilibria of mechanical models: application to dermal wound contraction. Mathematical Biosciences 1998, 147:113-129.
62. Olsen L., Maini P.K., Sherratt J.A., Dallon J.C. Mathematical modelling of anisotropy in fibrous connective tissue. Mathematical Biosciences 1999, 158:145-170.
63. Ramtani S. Mechanical modelling of cell/ecm and cell/cell interactions during the contraction of a fibroblast-populated collagen microsphere: theory and model simulation. Journal of Biomechanics 2004, 37:1709-1718.
64. Ramtani S., Fernandes-Morin E., Geiger D. Remodeled-matrix contraction by fibroblasts: numerical investigations. Computers in Biology and Medicine 2002, 32:283-296.
65. Reihsner R., Balogh B., Menzel E.J. Two-dimensional elastic properties of human skin in terms of incremental model at the in vivo configuration. Medical Engineering and Physics 1995, 17:3-4-313.
66. Rhett J.M., Ghatnekar G.S., Palatinus J.A., O'Quinn M., Yost M.J., Gourdie R.G. Novel therapies for scar reduction and regenerative healing of skin wounds. Trends in Biotechnology 2008, 26:173-180.
67. Roberts A.B., McCune B.K., Sporn M.B. Tgf-β: regulation of extracellular matrix. Kidney International 1992, 41:557-559.
68. Shreiber D.I., Barocas V.H., Tranquillo R.T. Temporal variations in cell migration and traction during fibroblast-mediated gel compaction. Biophysical Journal 2003, 84:4102-4114.
69. Shultz, G.S., Ladwig, G., Wysocki, A., 2005. Extracellular matrix: review of its roles in acute and chronic wounds. Published online at World Wide Wounds, URL: 〈〉. http://www.worldwidewounds.com/2005/august/Schultz/Extrace-Matric-Acute-Chronic-Wounds.html.
70. Sillman A.L., Quang D.M., Farboud B., Fang K.S., Nuccitelli R., Isseroff R.R. Human dermal fibroblasts do not exhibit directional migration on collagen 1 in direct-current electric fields of physiological strength. Experimental Dermatology 2003, 12:396-402.
71. Silver F.H., Freeman J.W., De Vore D. Viscoelastic properties of human skin and processed dermis. Skin Research and Technology 2001, 7:18-23.
72. Singer A.J., Clark R.A.F. Cutaneous wound healing. The New England Journal of Medicine 1999, 341:738-747.
73. Tamariz E., Grinnell F. Modulation of fibroblast morphology and adhesion during collagen matrix remodelling. Molecular Biology of the Cell 2002, 13:3915-3929.
74. Tracqui P., Woodward D.E., Cruywagen G.C., Cook J., Murray J.D. A mechanical model for fibroblast-driven wound healing. Journal of Biological Systems 1995, 3:1075-1084.
75. Tranqui L., Tracqui P. Mechanical signalling and angiogenesis. The integration of cell-extracellular matrix couplings. Life Sciences 2000, 323:31-47.
76. Tranquillo R.T., Murray J.D. Continuum model of fibroblast-driven wound contraction: inflammation-mediation. Journal of Theoretical Biology 1992, 158:135-172.
77. Vande Berg J.S., Rudolph R., Poolman W.L., Disharoon D.R. Comparative growth dynamics and active concentration between cultured human myofibroblasts from granulating wounds and dermal fibroblasts from normal skin. Laboratory Investigation 1989, 61:532-538.
78. Vermolen F.J., Javierre E. Computer simulations from a finite-element model for wound contraction and closure. Journal of Tissue Viability 2010, 19:43-53.
79. Wagenseil J.E., Okamoto R.J. Modeling cell and matrix anisotropy in fibroblast populated collagen vessels. Biomechanics and Modeling in Mechanobiology 2007, 6:151-162.
80. Wakatsuki T., Kolodney M.S., Zahalak G.I., Elson E.L. Cell mechanics studied by a reconstituted model tissue. Biophysical Journal 2000, 79:2353-2368.
81. Watts G.T. Wound shape and tissue tension in healing. The British Journal of Surgery 1960, 47:555-561.
82. Wells R.G., Discher D.E. Matrix elasticity, cytoskeletal tension, and tgf β: the insoluble and soluble meet. Science Signaling 2008, 1:pe13.
83. Wipff P.-J., Hinz B. Myofibroblasts work best under stress. Journal of Bodywork and Movement Therapies 2009, 13:121-127.
84. Wrobel L.K., Fray T.R., Molloy J.E., Adams J.J., Armitage M.P., Sparrow J.C. Contractility of single human dermal myofibroblasts and fibroblasts. Cell Motility and the Cytoskeleton 2002, 52:82-90.
85. Yang L., Qiu C.X., Ludlow A., Ferguson M.W.J., Brunner G. Active transforming growth factor-β in wound repair: determination using a new assay. American Journal of Pathology 1999, 154:105-111.
86. Zahalak G.I., Wagenseil J.E., Wakatsuki T., Elson E.L. A cell-based constitutive relation for bio-artificial tissues. Biophysical Journal 2000, 79:2369-2381.