In the beginning there were soft collagen-cell gels: Towards better 3D connective tissue models?

Experimental Cell Research

Volumn 319, Issue 16, 2013, Pages 2460-2469

  Brown, Robert A ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

3D tissue Models; Anisotropy; Collage engineering; Collagen plastic compression; Contraction contracture; Cross linking; Cytomechanics; Dupuytrens; Embossing; Fibril alignment; Fibril density; Fibril diameter; Fibroblast matrix continuum; Growth and ungrowth; Magnetic alignment; Measuring alignment; Mechanical alignment; Soft collagen gel

Indexed keywords

COLLAGEN GEL; INTEGRIN;

CONNECTIVE TISSUE; CONTRACTURE; DENSITY; EXTRACELLULAR MATRIX; FIBROBLAST; MORPHOGENESIS; PRIORITY JOURNAL; REVIEW; SCAR FORMATION; SKIN; TISSUE ENGINEERING; WOUND HEALING;

EID: 84883559642     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2013.07.001     Document Type: Review

References (89)

1. Elsdale T., Bard J. Collagen substrata for studies on cell behaviour. J. Cell Biol. 1972, 54:626-637.
2. Brown R.A. Asymmetry: 3D complexity and layer engineering. In, Extreme Tissue Engineering 2013, 131-161. John Wiley, Chichester, (ch.6).
3. Bell E., Ivarsson B., Merrill C. Production of a tissue-like structure by contraction of collagen lattices by human fibroblasts of different proliferative potential in vitro. Proc. Natl. Acad. Sci. USA 1979, 76:1274-1278.
4. Eaglstein W.H., Falanga V. Tissue engineering and development of Apligraf a human skin equivalent. Adv.Wound Care11 1998, 4(Suppl):1-8.
5. Falanga V. Apligraf treatment of venous ulcers and other chronic wounds. J. Dermatol. 1998, 25:812-817.
6. Tomasek J.J., Gabbiani G., Hinz B., Chaponnier C., Brown R.A. Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat. Rev. Mol. Cell Biol. 2002, 3:349-363.
7. Grinnell F., Petroll W.M. Cell motility and mechanics in three-dimensional collagen matrices. Ann. Rev. Cell Dev. Biol. 2010, 26:335-361.
8. Rhee S. Fibroblasts in three dimensional matrices: cell migration and matrix remodelling. Exp. Mol. Med. 2009, 41:858-865.
9. Dallon J.C., Ehrlich H.P. A review of fibroblast-populated collagen lattices. Wound Repair Regen. 2008, 16:472-479.
10. Carlson M.A., Longaker M.T. The fibroblast-populated collagen matrix as a model of wound healing: a review of the evidence. Wound Repair Regen. 2004, 12:134-147.
11. Friedl P., Bröcker E.B. The biology of cell locomotion within three-dimensional extracellular matrix. Cell Mol. Life Sci. 2000, 57:41-64.
12. Grinnell F. Fibroblast-collagen-matrix contraction: growth-factor signalling and mechanical loading. Trends Cell Biol. 2000, 10:362-365.
13. R.A.F.C.l.a.r.k., Nielsen L.D., Welch M.P., McPherson J.M. Collagen matrices attenuate the collagen-synthetic response of cultured fibroblasts to TGFbeta. J. Cell Sci. 1995, 108:1251-1261.
14. Arora P.D., Narani N., McCulloch C.A.G. The compliance of collagen gels regulates transforming growth factor beta induction of smooth muscle actin in fibroblasts. Am. J. Pathol. 1999, 154:871-882.
15. Komatsu I., Bond J., Selim A., Tomasek J.J., Levin L.S., Levinson H. Dupuytren's fibroblast contractility by sphingosine-1-phosphate is mediated through non-muscle myosin II. J. Hand Surg. Am. 2010, 35:1580-1588.
16. Parizi M., Howard E.W., Tomasek J.J. Regulation of LPA-promoted myofibroblast contraction Serum LPA and contraction: role of Rho, myosin light chain in kinase and myosin light chain phosphatase. Exp. Cell Res. 2000, 254:210-220.
17. Steinberg B.M., Smith K., Colozzo M., Pollack R. Establishment and transformation diminish the ability of fibroblasts to contract a native collagen gel. J. Cell Biol. 1980, 87:304-308.
18. Desmouliere A., Gabbiani G. Myofibroblast differentiation during fibrosis. Am. J. Pathol. 1995, 146:56-66.
19. Estes J.M., Vande Berg J.S., Adzick N.S., MacGillivray T.E., Desmouliere A., Gabbiani G. Phenotypic and functional features of myofibroblasts in sheep foetal wounds. Differentiation 1994, 56:173-181.
20. Brown R.A. Tissue engineering: clinical applications and mechanical control. In, Future Strategies for Tissue and Organ Replacement 2002, 51-78. Imperial College Press, London. J.M. Polak, L.L. Hench, P. Kemp (Eds.).
21. Karamichos D., Lakshman N., Petroll M.W. regulation of corneal fibroblast morphology and collagen re-organisation by extracellular matrix mechanical properties. Invest. Ophthalmol. Vis. Sci. 2007, 48:5030-5037.
22. Wakatsuki T., Elson E.L. Reciprocal interactions between cells and extracellular matrix during remodelling of tissue constructs. Biophys. Chem. 2003, 100:593-605.
23. Bellows C.G., Melcher A.H., Aubin J.E. Association between tension and orientation of periodontal ligament fibroblasts and exogenous collagen fibres in collagen gels in vitro. J. Cell Sci. 1982, 58:125-138.
24. Miron-Mendoza M., Seemann J., Grinnell F. The differential regulation of cell motile activity through matrix stiffness and porosity in three dimensional collagen matrices. Biomaterials 2010, 31:6425-6435.
25. Tomasek J.J., Haaksma C.J., Eddy R.J., Vaughan M.B. Fibroblast contraction occurs on release of tension in attached collagen lattices: dependency on an organized actin cytoskeleton and serum. Anat. Rec. 1992, 232:359-368.
26. Eastwood M., McGrouther D.A., Brown R.A. Fibroblast responses to mechanical forces. Proc. Inst. Mech. Eng. 1998, 212:85-92.
27. Eastwood M., McGrouther D.A., Brown R.A. Culture force monitor for measurement of contraction forces generated in human dermal fibroblast cultures. Biophys. Biochim. Acta. 1994, 1201:186-192.
28. Eastwood M., Mudera V.C., McGrouther D.A., Brown R.A. Effect of precise mechanical loading on fibroblast populated collagen lattices: morphological changes. Cell Motil. Cytoskeleton 1998, 40:13-21.
29. Kureshi A., Cheema U., Alekseeva T., Cambrey A., Brown R. Alignment hierarchies: engineering architecture from the nano-metre to the micro-metre scale. J. R. Soc. Interface 2010, S6:707-716.
30. Torbet J., Ronzière M.C. Magnetic alignment of collagen during self-assembly. Biochem. J. 1984, 219:1057-1059.
31. Guido S., Tranquillo R. A methodology for the systematic and quantitative study of contact guidance in orientated collagen gels. J.Cell Sci. 1993, 105:317-331.
32. Girton T.S., Barocas V.H., Tranquillo R.T. Confined compression of a tissue-equivalent: collagen fibril and cell alignment in response to anisotropic strain. J. Biomech. Eng. 2002, 125:568-575.
33. Kostyuk O., Brown R.A. Novel spectroscopic technique for in situ monitoring of collagen fibril alignment in gels. Biophys. J. 2004, 87:648-655.
34. Delvoye P., Wiliquet P., Leveque J., Nusgens B.V., Lapiere C.M. Measurement of mechanical forces generated by skin fibroblasts embedded in a 3D collagen Gel. J. Invest. Dermatol. 1991, 97:898-902.
35. Kolodney M.S., Wysolmerski R.B. Isometric contraction of fibroblasts and endothelial cells in tissue culture: a quantitative study. J. Cell Biol. 1992, 117:73-82.
36. Thomopoulos S., Das R., Birman V., et al. Fibrocartilage tissue engineering: the role of the stress environment on cell morphology and matrix expression. Tissue Eng. A. 2011, 17:1039-1053.
37. Wakatsuki T., Kolodney M.S., Zahalak Z.I., Elson E.L. Cell Mechanics studied by a reconstituted model tissue. Biophys. J. 2000, 79:2353-2368.
38. Fernandez P., Bausch A.R. The compaction of gels by cells: a case of collective mechanical activity. Integr. Biol. 2009, 1:252-259.
39. Harris A.K., Stopak D., Wild P. Fibroblast traction as a mechanism for collagen morphogenesis. Nature 1981, 290:249-251.
40. Lo C.M., Wang H.B., Dembo M., Wang Y.L. Cell movement is guided by the rigidity of the substrate. Biophys. J. 2000, 79:144-152.
41. Brown R.A., Pajapati R., McGrouther D.A., Yannas I.V., Eastwood M. Tensional homeostasis in dermal fibroblasts: mechanical respones to mechanical loading in 3-dimensional substrates. J.Cell Physiol. 1998, 175:323-332.
42. Levinson H., Turner C.E., Ehrlich H.P. Integrin-linked kinase: a possible role in scar contracture. Ann.Plast.Surg. 2004.
43. Karamichos D., Brown R.A., Mudera V. Complex dependence of substrate stiffness and serum concentration on cell-force generation. J. Biomed. Mater. Res. Part A. 2007, 83:887-894.
44. Porter R.A., Brown R.A., Eastwood M., Khaw P., Occelston N. Ultra-structural changes during contraction of collagen lattices by ocular fibroblasts. Wound Repair Regen. 1998, 6:157-166.
45. Lee T.L., Lin Y.C., Mochitate K., Grinnell F. Stress-relaxation of fibroblasts in collagen matrices triggers exocytosis of plasma membrane vesicles containing actin, annexins II and VI and beta 1 integrin receptors. J.Cell Sci. 1993, 105:167-177.
46. Eguchi Y., Ogiue-Ikeda M., Ueno S. Control of orientation of rat Schwann cells using an 8-T static magnetic field. Neurosci. Lett. 2003, 351:130-132.
47. Mudera V.C., Pleass R., Eastwood M., Tarnuzzer R., Schultz G., Khaw P., McGrouther D.A., Brown R.A. Molecular responses of human dermal fibroblasts to dual cues: contact guidance and mechanical load. Cell Motil Cytoskeleton 2000, 45:1-9.
48. Jenkins G., Redwood K.L., Meadows L., Green M.r. Effect of gel reorganisation and tensional forces on alpha 2 beta 1 integrin levels in dermal fibroblasts. Eur. J. Biochem. 1999, 263:93-103.
49. Marenzana M., Wilson-Jones N., Mudera V., Brown R.A. The origins and regulation of tissue tension: identification of collagen tension-fixation process in vitro. Exp. Cell Res. 2006, 312:423-433.
50. R.A. Brown, Direct collagen-material engineering for tissue fabrication, Tissue Eng. A. March 21st 2013 (Epub ahead of print).
51. Mosse G., Anglo A., Helary C., Bouligand Y., Giraud-Guille M.M. Dense tissue-like collagen matrices formed in cell-free conditions. Matrix Biol 2006, 25:3-13.
52. Helary C., Foucault-Bertaud A., Godeau G., Coulomb B., Giraud-Guille M.M. Fibroblast populated dense collagen matrices: cell migration, cell density and metalloproteinase expression. Biomaterials 2005, 26:1533-1543.
53. Badylak S.F. The extracellular matrix as a scaffold for tissue reconstruction. Semin. Cell Dev. Biol. 2002, 13:377-383.
54. Krishnan L., Weiss J.A., Wessman M.D., Hoying J.B. Design and application of a test system for viscoelastic characterisation of collagen gels. Tissue Eng. 2004, 10:241-252.
55. Brown R.A., Wiseman M., Chuo C.-B., Cheema U., Nazhat S.N. Ultrarapid engineering of biomimetic materials and tissues: fabrication of nano- and microstructures by plastic compression. Adv. Funct. Mater. 2005, 15:1762-1770.
56. Abou-Neel E.A., Cheema U., Knowles J.C., Brown R.A., Nazhat S.N. Use of multiple unconfined compression for control of collagen gel scaffold mechanical properties. Soft Matter 2006, 2:986-992.
57. Bitar M., Salih V., Brown R.A., Nazhat S.N. Effect of multiple unconfined compression on cellular dense collagen scaffolds for bone tissue engineering. J. Mater. Sci. 2007, 18:237-244.
58. Cheema U., Alp B., Faroughi F., Anandagoda N., Mudera V., Nazhat S.N., Brown R.A. Fabricating tissues: review of farming versus engineering strategies. Biotech. Bioprocess Eng. 2007, 12:9-14.
59. Anandagoda N., Ezra D.G., Cheema U., Bailly M., Brown R.A. Hyaluronan hydration generates 3d meso-scale structure in engineered collagen tissues. J. Roy.Soc. Interface 2012, 9:2680-2687.
60. T. Alekseeva, H. Jawad, M. Purser, R.A. Brown, New improved technique for plastic compression of collagen using upward flow, in: Proceedings of the IFMBE, vol 30, 2011, pp. 5-8.
61. Hu K., Shi H., Deng D., Zhou G., Cao Y., Lui W. Compressed collagen gel as the scaffold for skin engineering. Biomed. Microdevices 2010, 12:627-635.
62. Hadjipanyi E., Mudera V., Brown R.A. Close dependence of fibroblast growth and collagen scaffold matrix stiffness. J.Tissue Eng.Regen.Med. 2009, 3:77-84.
63. Hadjipanyi E., Mudera V., Brown R.A. Guided cell migration in 3D: a collagen matrix with graded directional stiffness. Cell Motil. Cytoskeleton 2009, 66:121-128.
64. Jiang G., Huang A.H., Cai Y., Tanase M., Sheetz M.P. Rigidity sensing at the leading edge through alphaV beta3 integrins and RPTP alpha. Biophys. J. 2006, 90:1804-1809.
65. Isenberg B.C., Dimilla P.A., Walker M., Kim S., Wong J.Y. Vascular smooth muscle cell durotaxis depends on substrate stiffness gradient strength. Biophys. J. 2009, 97:1313-1322.
66. Mudera V., Morgan M., Cheema U., Nazhat S.N., Brown R.A. Ultra-rapid engineered collagen constructs tested in an in vivo nursery site. J.Tissue Eng.Regen Med. 2007, 1:192-198.
67. Hadjipanyi E., Mudera V., Deng D., Liu W., Cheema U., Brown R.A. First implantable device for hypoxia-induced angiogenic engineering. J.Controlled Release 2011, 153:217-224.
68. Cheema U., Chuo C.-B., Sarathchandra P., Nazhat S.N., Brown R.A. Engineering functional collagen scaffolds: cyclical loading increases material strength and fibril aggregation. Adv. Funct. Mater. 2007, 17:2426-2431.
69. Dubey N., Letourneau P.C., Tranquillo R.T. Guided neurite elongation and schwann cell invasion into magnetically aligned collagen in simulated peripheral nerve regeneration. Exp. Neurol. 1999, 158:338-350.
70. Dalby M.J., Riehle M.O., Yrawood S.J., Wilkinson C.D., Curtis A.S. Nucleus alignment and cell signalling in fibroblasts: response to micro-grooved topography. Exp.Cell Res. 2003, 284:274-282.
71. Ceballos D., Navarro X., Dubey N., Wendelschafer-Crabb G., Kennedy W.R., Tranquillo R.T. Magnetically aligned collagen gel filling a collagen nerve guide improves peripheral nerve regeneration. Exp. Neurol. 1999, 158:290-300.
72. Ahearne M., Bagnaninchi P.O., Yang Y., El Haj A.J. Online monitoring of collagen fibre alignment in tissue engineered tendon by PSOCT. J.Tissue Eng. Regen. Med. 2008, 2:521-524.
73. Giraude-Guille M.M. Twisted liquid crystalline supramolecular arrangements in morphogenesis. Int. Rev. Cytol. 1996, 166:59-101.
74. Guo C., Kaufman L.J. Flow and magnetic field induced collagen alignment. Biomaterials 2007, 28:1105-1114.
75. Xu B., Chow M.J., Zhang Y. Experimental and modelling study of collagen scaffolds with the effects of cross-linking and fibre alignment. Int. J. Biomater 2011, 2011:172389.
76. East E., de Oliveira D.B., Goldring J.P., Phillips J.B. Alignment of astrocytes increases neural growth in 3D collagen gels and is maintained following plastic compression to form a spinal repair conduit. Tissue Eng. A. 2012, 16:3173-3184.
77. Phillips J.B., Bunting S.C., Hall S.M., Brown R.A. Neural tissue engineering: a self organising collagen guidance conduit. Tissue Eng. 2005, 11:1611-1617.
78. Torbet J., Malbouyres M., Builles N., Justin V., Roulet M., Damour O., Oldberg A., Ruggiero F., Holmes D.J. Orthogonal scaffold of magnetically aligned collagen lamellae for corneal stroma reconstruction. Biomaterials 2007, 28:4268-4276.
79. Alekseeva T., Hadjipanayi E., Abou Neel E.A., Brown R.A. Engineering stable topography in dense bio-mimetic 3D collagen scaffolds. Eur. Cell Mater. 2012, 23:28-40.
80. Nazhat S.N., et al. Controlled micro-channeling in dense collagen gels by degrading glass fibres. Biomacromolecules 2007, 8:543-551.
81. Alekseeva T., Hadjipanayi E., Abou Neel E.A., Brown R.A. Engineering stable topography in dense bio-mimetic 3D collagen scaffolds. Eur. Cell Mater. 2012, 23:28-40.
82. Wong J., MacRobert A.J., Cheema U., Brown R.A. Mechanical anisotropy in compressed collagen produced by localised photo-cross-linking. J. Mech. Behav. Biomed. Mater. 2013, 18:132-139.
83. Aherne M., Yang Y., Then K.Y., Liu K.K. Non-destructive mechanical characterisation of UVA/ribofalvin cross-linked collagen hydrogels. Br.J.Ophthamol. 2008, 92:268-271.
84. Oban J.M., Wilson L.B., Kofroth J.A., El-Kurdi M.S., Maul T.M., Vorp D.A. Crosslinking of collagen gels with transglutaminase. J.Biomed.Mater.Res. A. 2004, 68:756-762.
85. Chen R.N., Ho H.O., Sheu M.T. Characterisation of collagen matrices cross-linked using microbial transglutaminase. Biomaterials 2005, 26:4229-4235.
86. Zeuglois D.I., Panengad P.P., Yew E.S., Shepphard C., Phan T.T., Raghunath M. An in situ and in vitro investigation for the transglutaminase potential in tissue engineering. J.Biomed.Mater.Res. A 2010, 92:1310-1320.
87. Sundararaghaven H.G., Monteiro G.A., Firestein B.L., Shreiber D.I. Neurite growth in 3D collagen gels with gradients of mechanical properties. Biotech. Bioeng. 2009, 102:632-643.
88. Carlson M.A., Longaker M.T. The fibroblast populated collagen matrix as a model of wound healing: a review of the evidence. Wound Rep. Regen. 2004, 12:134-147.
89. Brown R.A. Other ways to grow tissues? In, Extreme Tissue Engineering 2013, 163-183. John Wiley, Chichester, (ch.7).