Online monitoring of the mechanical behavior of collagen hydrogels: Influence of corneal fibroblasts on elastic modulus

Tissue Engineering - Part C: Methods

Volumn 16, Issue 2, 2010, Pages 319-327

  Ahearne, Mark ^a   Liu, Kuo Kang ^a   El Haj, Alicia J ^a   Then, Kong Y ^b   Rauz, Saaeha ^b   Yang, Ying ^a  

^a KEELE UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMECHANICS; COLLAGEN; ELASTIC MODULI; ENZYME INHIBITION; FIBROBLASTS; HYDROGELS; MATHEMATICAL MODELS; MECHANICAL PROPERTIES; MECHANISMS; PARTIAL DISCHARGES;

ACTIN POLYMERIZATION; CELL BEHAVIORS; CHEMICAL REAGENTS; CORNEAL FIBROBLASTS; FEED-BACK LOOP; HUMAN CORNEAL; IN-VITRO; MATRIX METALLOPROTEINASES; MECHANICAL BEHAVIOR; MECHANICAL CHARACTERISTICS; MECHANICAL PROPERTIES OF CELLS; ONLINE MONITORING; ONLINE MONITORING TECHNIQUE; SPHERICAL INDENTATIONS; SURROUNDING MATRIX; TENSILE FORCES;

CELL CULTURE;

COLLAGEN; CYTOCHALASIN D;

ARTICLE; BIOMECHANICS; CELL COUNT; CELL CULTURE; CELL PROLIFERATION; CHEMISTRY; CORNEA; CULTURE TECHNIQUE; CYTOLOGY; DRUG EFFECT; EVALUATION; FIBROBLAST; HUMAN; HYDROGEL; INSTRUMENTATION; METHODOLOGY; MONITORING; ONLINE SYSTEM; PHYSIOLOGY; YOUNG MODULUS;

BIOMECHANICS; CELL COUNT; CELL CULTURE TECHNIQUES; CELL PROLIFERATION; CELLS, CULTURED; COLLAGEN; CORNEA; CYTOCHALASIN D; ELASTIC MODULUS; FIBROBLASTS; HUMANS; HYDROGELS; MONITORING, PHYSIOLOGIC; ONLINE SYSTEMS;

EID: 77952347215     PISSN: 19373384     EISSN: 19373392     Source Type: Journal    
DOI: 10.1089/ten.tec.2008.0650     Document Type: Article

References (42)

1. Reichl, S., Bednarz, J., and Muller-Goymann, C.C. Human corneal equivalent as cell culture model for in vitro drug permeation studies. Br J Ophthalmol 88, 560, 2004.
2. Ahearne, M., Yang, Y., Then, K.Y., and Liu, K.K. Nondestructive mechanical characterization of UVA=riboflavin crosslinked collagen hydrogels. Br J Ophthalmol 92, 268, 2008.
3. Sandeman, S.R., Allen, M.C., Liu, C., Faragher, R.G.A., and Lloyd, A.W. Human keratocyte migration into collagen gels declines with in vitro aging. Mech Ageing Dev 119, 149, 2000.
4. Eastwood, M., McGrouther, D.A., and Brown, R.A. A culture force monitor for measurement of contraction forces generated in human dermal fibroblast cultures: evidence for cell-matrix mechanical signalling. Biochem Biophys Acta 1201, 186, 1994.
5. Shi-Wen, X., Denton, C.P., Dashwood, M.R., Holmes, A.M., Bou-Gharios, G., Pearson, J.D., Black, C.M., and Abraham, D.J. Fibroblast matrix gene expression and connective tissue remodeling: role of endothelin-1. J Invest Dermatol 116, 417, 2001.
6. Sethi, K.K., Yannas, I.V., Mudera, V., Eastwood, M., McFarland, C., and Brown, R.A. Evidence for sequential utilization of fibronectin, vitronectin, and collagen during fibroblast-mediated collagen contraction. Wound Rep Reg 10, 397, 2002.
7. Freyman, T.M., Yannas, I.V., Yokoo, R., and Gibson, L.J. Fibroblast contraction of a collagen-GAG matrix. Biomater-ials 22, 2883, 2001.
8. Freyman, T.M., Yannas, I.V., Yokoo, R., and Gibson, L.J. Fibroblast contractile force is independent of the stiffness which resists the contraction. Exp Cell Res 272, 153, 2002.
9. Bell, E., Ivarsson, B., and Merrill, C. Production of a tissuelike structure by contraction of collagen lattices by human fibroblasts of different proliferative potential in vitro. Proc Natl Acad Sci USA 76, 1274, 1979.
10. Dans, M.J., and Isseroff, R. Inhibition of collagen lattice contraction by pentoxifylline and interferon-alpha,-beta, and-gamma. J Invest Dermatol 102, 118, 1994.
11. Ahearne, M., Yang, Y., El Haj, A.J., Then, K.Y., and Liu, K.K. Characterizing the viscoelastic properties of thin hydrogel-based constructs for tissue engineering applications. J R Soc Interface 2, 455, 2005.
12. Ju, B.F., and Liu, K.K. Characterizing viscoelastic properties of thin elastomeric membrane. Mech Mater 34, 485, 2002.
13. Anseth, K.S., Bowman, C.N., and Brannon-Peppas, L. Mechanical properties of hydrogels and their experimental determination. Biomaterials 17, 1647, 1996.
14. Bagnaninchi, P.O., Yang, Y., Zghoul, N., Maffulli, N., Wang, R.K., and El Haj, A.J. Chitosan microchannel scaffolds for tendon tissue engineering characterized using optical coherence tomography. Tissue Eng 13, 323, 2007.
15. Yang, Y., Bagnaninchi, P.O., Ahearne, M., Wang, R.K., and Liu, K.K. A novel optical coherence tomography-based micro-indentation technique for mechanical characterization of hydrogels. J R Soc Interface 4, 1169, 2007.
16. Galardy, R.E., Cassabonne, M.E., Giese, C., Gilbert, J.H., Lapierre, F., Lopez, H., Schaefer, M.E., Stack, R., Sullivan, M., Summers, B., Tressler, R., Tyrrell, D., Wee, J., Allen, S.D., Castellot, J.J., Barletta, J.P., Schultz, G.S., Fernandez, L.A., Fisher, S., Cui, T., Foellmer, H.G., Grobelny, D., and Hiller-an, W.M. Low molecular weight inhibitors in corneal ul-ceration. Ann NY Acad Sci 732, 315, 1994.
17. Vishwanath, M., Ma, L., Otey, C.A., Jester, J.V., and Petroll, W.M. Modulation of corneal fibroblast contractility within fibrillar collagen matrices. Invest Ophthalmol Vis Sci 44, 4724, 2003.
18. Petroll, W.M., Vishwanath, M., and Ma, L. Corneal fibro-blasts respond rapidly to changes in local mechanical stress. Invest Ophthalmol Vis Sci 45, 3466, 2004.
19. Brown, R. Cytomechanics in connective tissue repair and engineering. In: Chaponnier, C., Desmouliere, A., and Gab-biani, G., eds. Tissue Repair, Contraction and the Myofi-broblast. New York: Springer, 2006, pp. 7-24.
20. Isenberg, G., Rathke, P.C., Hulsmann, N., Franke, W.W., and Wohlfarth-Bottermann, K.E. Cytoplasmic actomyosin fibrils in tissue culture cells: direct proof of contractility by visualization of ATP-induced contraction in fibrils isolated by laser micro-beam dissection. Cell Tissue Res 166, 427, 1976.
21. Discher, D.E., Janmey, P., and Wang, Y.L. Tissue cells feel and respond to the stiffness of their substrate. Science 310, 1139, 2005.
22. Abou Neel, E.A., Cheema, U., Knowles, J.C., Brown, R.A., and Nazhat, S.N. Use of multiple unconfined compression for control of collagen gel scaffold density and mechanical properties. Soft Matter 2, 986, 2006.
23. Saddiq, Z.A., Barbenel, J.C., and Grant, M.H. The mechanical strength of collagen gels containing glycosaminoglycans and populated with fibroblasts. J Biomed Mater Res A 89, 697, 2009.
24. Daniels, J.T., Cambrey, A.D., Occleston, N.L., Garrett, Q., Tarnuzzer, R.W., Schultz, G.S., and Khaw, P.T. Matrix me-talloproteinase inhibition modulates fibroblast-mediated matrix contraction and collagen production in vitro. Invest Ophthalmol Vis Sci 44, 1104, 2003.
25. Pilcher, B.K., Dumin, J.A., Sudbeck, B.D., Krane, S.M., Wel-gus, H.G., and Parks, W.C. The activity of collagenase-1 is required for keratinocyte migration on a type I collagen matrix. J Cell Biol 137, 1445, 1997.
26. Raeber, G.P., Lutolf, M.P., and Hubbell, J.A. Mechanisms of 3-D migration and matrix remodeling of fibroblasts within artificial ECMs. Acta Biomater 3, 615, 2007.
27. Wozniak, M.A., Desai, R., Solski, P.A., Der, C.J., and Keely, P.J. ROCK-generated contractility regulates breast epithelial cell differentiation in response to the physical properties of a three-dimensional collagen matrix. J Cell Biol 163, 583, 2003.
28. Engler, A.J., Sen, S., Sweeney, H.L., and Discher, D.E. Matrix elasticity directs stem cell lineage specification. Cell 126, 677, 2006.
29. Karamichos, D., Brown, R.A., and Mudera, V. Collagen stiffness regulates cellular contraction and matrix remodeling gene expression. J Biomed Mater Res A 83, 887, 2007.
30. Wakatsuki, T., and Elson, E.L. Reciprocal interactions between cells and extracellular matrix during remodeling of tissue constructs. Biophys Chem 100, 593, 2003.
31. Farahani, R.M., and Kloth, L.C. The hypothesis of "biophysical matrix contraction": wound contraction revisited. Int Wound J 5, 477, 2008.
32. Cheng, G., Tse, J., Jain, R.K., and Munn, L.L. Micro-environmental mechanical stress controls tumor spheroid size and morphology by suppressing proliferation and inducing apoptosis in cancer cells. PLoS One 4, e4632, 2009.
33. Gefen, A., van Nierop, B., Bader, D.L., and Oomens, C.W. Strain-time cell-death threshold for skeletal muscle in a tissue-engineered model system for deep tissue injury. J Biomech 41, 2003, 2008.
34. Moore, M.M., Goldman, J., Patel, A.R., Chien, S., and Liu, S.Q. Role of tensile stress and strain in the induction of cell death in experimental vein grafts. J Biomech 34, 289, 2001.
35. Fluck, J., Querfeld, C., Cremer, A., Niland, S., Krieg, T., and Sollberg, S. Normal human primary fibroblasts undergo apoptosis in three-dimensional contractile collagen gels. J Invest Dermatol 110, 153, 1998.
36. Goldman, J., Zhong, L., and Liu, S.Q. Degradation of alpha-actin filaments in venous smooth muscle cells in response to mechanical stretch. Am J Physiol Heart Circ Physiol 284, H1839, 2003.
37. White, S.R., Williams, P., Wojcik, K.R., Sun, S., Hiemstra, P.S., Rabe, K.F., and Dorscheid, D.R. Initiation of apoptosis by actin cytoskeletal derangement in human airway epithelial cells. Am J Respir Cell Mol Biol 24, 282, 2001.
38. Grinnell, F., Zhu, M.F., Carlson, M.A., and Abrams, J.M. Release of mechanical tension triggers apoptosis of human fibroblasts in a model of regressing granulation tissue. Exp Cell Res 248, 608, 1999.
39. Niland, S., Cremer, A., Fluck, J., Eble, J.A., Krieg, T., and Sollberg, S. Contraction-dependent apoptosis of normal dermal fibroblasts. J Invest Dermatol 116, 686, 2001.
40. Stuart, P.M., Pan, F., Yin, X., Haskova, Z., Plambeck, S., and Ferguson, T.A. Effect of metalloprotease inhibitors on corneal allograft survival. Invest Ophthalmol Vis Sci 45, 1169, 2004.
41. Schultz, G.S., Strelow, S., Stern, G.A., Chegini, N., Grant, M.B., Galardy, R.E., Grobelny, D., Rowsey, J.J., Stonecipher, K., and Parmley, V. Treatment of alkali-injured rabbit corneas with a synthetic inhibitor of matrix metalloproteinases. Invest Ophthalmol Vis Sci 33, 3325, 1992.
42. Wong, T.T.L., Mead, A.L., and Khaw, P.T. Matrix metallo-proteinase inhibition modulates postoperative scarring after experimental glaucoma filtration surgery. Invest Ophthal-mol Vis Sci 44, 1097, 2003.