Development of a three-dimensional human skin equivalent wound model for investigating novel wound healing therapies

Tissue Engineering - Part C: Methods

Volumn 16, Issue 5, 2010, Pages 1111-1123

  Xie, Yan ^a   Rizzi, Simone C ^a   Dawson, Rebecca ^a   Lynam, Emily ^a   Richards, Sean ^a   Leavesley, David I ^a   Upton, Zee ^a  

^a QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

MAMMALS; OPTIMIZATION; REPAIR; THREE DIMENSIONAL;

CLINICAL TRIAL; EX-VIVO; HUMAN SKIN; NEW MODEL; PHYSIOLOGICAL DIFFERENCES; PRECLINICAL STUDIES; SMALL ANIMAL MODEL; WOUND HEALING; WOUND HEALING PROCESS; WOUND REPAIR;

PHYSIOLOGICAL MODELS;

ANIMALIA; RODENTIA; SUIDAE;

ARTICLE; CELL CULTURE; FLUORESCENT ANTIBODY TECHNIQUE; HUMAN; PATHOLOGY; REPRODUCIBILITY; SKIN; VALIDATION STUDY; WOUND HEALING;

CELLS, CULTURED; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; REPRODUCIBILITY OF RESULTS; SKIN; WOUND HEALING;

EID: 77957373159     PISSN: 19373384     EISSN: 19373392     Source Type: Journal    
DOI: 10.1089/ten.tec.2009.0725     Document Type: Article

References (54)

1. Moulin, V., Auger, F.A., Garrel, D., and Germain, L. Role of wound healing myofibroblasts on re-epithelialization of human skin. Burns 26, 3, 2000.
2. Gottrup, F., Agren, M.S., and Karlsmark, T. Models for use in wound healing research: a survey focusing on in vitro and in vivo adult soft tissue. Wound Repair Regen 8, 83, 2000.
3. Regnier, M., Asselineau, D., and Lenoir, M.C. Human epidermis reconstructed on dermal substrates in vitro: an alternative to animals in skin pharmacology. Skin Pharmacol 3, 70, 1990.
4. Chakrabarty, K.H., Dawson, R.A., Harris, P., Layton, C., Babu, M., Gould, L., Phillips, J., Leigh, I., Green, C., Freed-lander, E., and Mac Neil, S. Development of autologous human dermal-epidermal composites based on sterilized human allodermis for clinical use. Br J Dermatol 141, 811, 1999.
5. Song, J., Izumi, K., Lanigan, T., and Feinberg, S.E. Development and characterization of a canine oral mucosa equivalent in a serum-free environment. J Biomed Mater Res 71, 143, 2004.
6. Boyce, S., Michel, S., Reichert, U., Shroot, B., and Schmidt, R. Reconstructed skin from cultured human keratinocytes and fibroblasts on a collagen-glycosaminoglycan biopolymer substrate. Skin Pharmacol 3, 136, 1990.
7. Gangatirkar, P., Paquet-Fifield, S., Li, A., Rossi, R., and Kaur, P. Establishment of 3D organotypic cultures using human neonatal epidermal cells. Nat Protoc 2, 178, 2007.
8. Parenteau, N., Sabolinski, M., Prosky, S., Nolte, C., Oleson, M., Kriwet, K., and Bilbo, P. Biological and physical factors influencing the successful engraftment of a cultured human skin substitute. Biotechnol Bioeng 52, 3, 1996.
9. Zacchi, V., Soranzo, C., Cortivo, R., Radice, M., Brun, P., and Abatangelo, G. In vitro engineering of human skin-like tissue. J Biomed Mater Res 40, 187, 1998.
10. Pianigiani, E., Andreassi, A., Taddeucci, P., Alessandrini, C., Fimiani, M., and Andreassi, L. A new model for studying differentiation and growth of epidermal cultures on hyaluronan-based carrier. Biomaterials 20, 1689, 1999.
11. Ralston, D.R., Layton, C., Dalley, A.J., Boyce, S.G., Freed-lander, E., and MacNeil, S. Keratinocytes contract human dermal extracellular matrix and reduce soluble fibronectin production by fibroblasts in a skin composite model. Br J Plast Surg 50, 408, 1997.
12. Legrand, C., Polette, M., Tournier, J.M., de Bentzmann, S., Huet, E., Monteau, M., and Birembaut, P. uPA=plasmin system-mediated MMP-9 activation is implicated in bronchial epithelial cell migration. Exp Cell Res 264, 326, 2001.
13. Oberringer, M., Meins, C., Bubel, M., and Pohlemann, T. A new in vitro wound model based on the co-culture of human dermal microvascular endothelial cells and human dermal fibroblasts. Biol Cell 99, 197, 2007.
14. Reed, J.T., Ghadially, R., and Elias, P.M. Skin type, but neither race nor gender, influence epidermal permeability barrier function. Arch Dermatol 131, 1134, 1995.
15. Cribbs, R.K., Luquette, M.H., and Besner, G.E. A standardized model of partial thickness scald burns in mice. J Surg Res 80, 69, 1998.
16. Topping, G., Malda, J., Dawson, R., and Upton, Z. Development and characterisation of human skin equivalents and their potential application as a burn wound model. Primary Intention 14, 14, 2006.
17. Pilcher, B.K., Dumin, J., Schwartz, M.J., Mast, B.A., Schultz, G.S., Parks, W.C., and Welgus, H.G. Keratinocyte collagenase-1 expression requires an epidermal growth factor receptor autocrine mechanism. J Biol Chem 274, 10372, 1999.
18. Blank, I.H., and Miller, O.G. A method for the separation of the epidermis from the dermis. J Invest Dermatol 15, 9, 1950.
19. Middelkoop, E., van den Bogaerdt, A.J., Lamme, E.N., Hoekstra, M.J., Brandsma, K., and Ulrich, M.M. Porcine wound models for skin substitution and burn treatment. Biomaterials 25, 1559, 2004.
20. Sams, H.H., McDonald, M.A., and Stasko, T. Useful adjuncts to harvest split-thickness skin grafts. Dermatol Surg 30, 1591, 2004.
21. Egles, C., Shamis, Y., Mauney, J.R., Volloch, V., Kaplan, D.L., and Garlick, J.A. Denatured collagen modulates the pheno-type of normal and wounded human skin equivalents. J Invest Dermatol 128, 1830, 2008.
22. El Ghalbzouri, A., Hensbergen, P., Gibbs, S., Kempenaar, J., van der Schors, R., and Ponec, M. Fibroblasts facilitate re-epithelialization in wounded human skin equivalents. Lab Invest 84, 102, 2004.
23. Geer, D.J., Swartz, D.D., and Andreadis, S.T. Fibrin promotes migration in a three-dimensional in vitro model of wound regeneration. Tissue Eng 8, 787, 2002.
24. Lee, J.P., Jalili, R.B., Tredget, E.E., Demare, J.R., and Ghah-ary, A. Antifibrogenic effects of liposome-encapsulated IFN-alpha2b cream on skin wounds in a fibrotic rabbit ear model. J Interferon Cytokine Res 25, 627, 2005.
25. Falanga, V., Isaacs, C., Paquette, D., Downing, G., Kouttab, N., Butmarc, J., Badiavas, E., and Hardin-Young, J. Wounding of bioengineered skin: cellular and molecular aspects after injury. J Invest Dermatol 119, 653, 2002.
26. Harrison, C.A., Heaton, M.J., Layton, C.M., and Mac Neil, S. Use of an in vitro model of tissue-engineered human skin to study keratinocyte attachment and migration in the process of reepithelialization. Wound Repair Regen 14, 203, 2006.
27. Geer, D.J., Swartz, D.D., and Andreadis, S.T. In vivo model of wound healing based on transplanted tissue-engineered skin. Tissue Eng 10, 1006, 2004.
28. Kratz, G. Modeling of wound healing processes in human skin using tissue culture. Microsc Res Tech 42, 345, 1998.
29. Laplante, A.F., Germain, L., Auger, F.A., and Moulin, V. Mechanisms of wound reepithelialization: hints from a tissue-engineered reconstructed skin to long-standing questions. FASEB J 15, 2377, 2001.
30. Moll, I., Houdek, P., Schmidt, H., and Moll, R. Characterization of epidermal wound healing in a human skin organ culture model: acceleration by transplanted keratinocytes. J Invest Dermatol 111, 251, 1998.
31. Schneider, A., Garlick, J.A., and Egles, C. Self-assembling peptide nanofiber scaffolds accelerate wound healing. PLoS ONE 3, e1410, 2008.
32. Stephens, P., Wood, E.J., and Raxworthy, M.J. Development of a multilayered in vitro model for studying events associated with wound healing. Wound Repair Regen 4, 393, 1996.
33. Vaughan, M.B., Ramirez, R.D., Brown, S.A., Yang, J.C., Wright, W.E., and Shay, J.W. A reproducible laser-wounded skin equivalent model to study the effects of aging in vitro. Rejuvenation Res 7, 99, 2004.
34. Rheinwald, J.G., and Green, H. Serial cultivation of strains of human epidermal keratinocytes: the formation of keratiniz-ing colonies from single cells. Cell 6, 331, 1975.
35. Dawson, R.A., Upton, Z., Malda, J., and Harkin, D.G. Preparation of cultured skin for transplantation using insulinlike growth factor I in conjunction with insulin-like growth factor binding protein 5, epidermal growth factor, and vitronectin. Transplantation 81, 1668, 2006.
36. Ehrbar, M., Rizzi, S.C., Hlushchuk, R., Djonov, V., Zisch, A.H., Hubbell, J.A., Weber, F.E., and Lutolf, M.P. Enzymatic formation of modular cell-instructive fibrin analogs for tissue engineering. Biomaterials 28, 3856, 2007.
37. Ehrbar, M., Rizzi, S.C., Schoenmakers, R.G., Miguel, B.S., Hubbell, J.A., Weber, F.E., and Lutolf, M.P. Biomolecular hydrogels formed and degraded via site-specific enzymatic reactions. Biomacromolecules 8, 3000, 2007.
38. Upton, Z., Cuttle, L., Noble, A., Kempf, M., Topping, G., Malda, J., Xie, Y., Mill, J., Harkin, D.G., Kravchuk, O., Lea-vesley, D.I., and Kimble, R.M. Vitronectin: growth factor complexes hold potential as a wound therapy approach. J Invest Dermatol 128, 1535, 2008.
39. Breetveld, M., Richters, C.D., Rustemeyer, T., Scheper, R.J., and Gibbs, S. Comparison of wound closure after burn and cold injury in human skin equivalents. J Invest Dermatol 126, 1918, 2006.
40. Odland, G., and Ross, R. Human wound repair. I. Epidermal regeneration. J Cell Biol 39, 135, 1968.
41. Richards, S., Leavesley, D., Topping, G., and Upton, Z. Development of defined media for the serum-free expansion of primary keratinocytes and human embryonic stem cells. Tissue Eng Part C Methods 14, 221, 2008.
42. Bhora, F.Y., Dunkin, B.J., Batzri, S., Aly, H.M., Bass, B.L., Sidawy, A.N., and Harmon, J.W. Effect of growth factors on cell proliferation and epithelialization in human skin. J Surg Res 59, 236, 1995.
43. Andreadis, S.T., Hamoen, K.E., Yarmush, M.L., and Morgan, J.R. Keratinocyte growth factor induces hyperproliferation and delays differentiation in a skin equivalent model system. FASEB J 15, 898, 2001.
44. Sun, T., Jackson, S., Haycock, J.W., and MacNeil, S. Culture of skin cells in 3D rather than 2D improves their ability to survive exposure to cytotoxic agents. J Biotechnol 122, 372, 2006.
45. Birgersdotter, A., Sandberg, R., and Ernberg, I. Gene expression perturbation in vitro\a growing case for three-dimensional (3D) culture systems. Semin Cancer Biol 15, 405, 2005.
46. Weaver, V.M., Petersen, O.W., Wang, F., Larabell, C.A., Briand, P., Damsky, C., and Bissell, M.J. Reversion of the malignant phenotype of human breast cells in three-dimensional culture and in vivo by integrin blocking antibodies. J Cell Biol 137, 231, 1997.
47. Herbert, C.B., Bittner, G.D., and Hubbell, J.A. Effects of fi-binolysis on neurite growth from dorsal root ganglia cultured in two-and three-dimensional fibrin gels. J Comp Neurol 365, 380, 1996.
48. Pepper, M.S. Role of the matrix metalloproteinase and plasminogen activator-plasmin systems in angiogenesis. Arterioscler Thromb Vasc Biol 21, 1104, 2001.
49. Raeber, G.P., Lutolf, M.P., and Hubbell, J.A. Molecularly engineered PEG hydrogels: a novel model system for pro-teolytically mediated cell migration. Biophys J 89, 1374, 2005.
50. Gilje, O. On taping (adhesive tape treatment) of leg ulcers. Acta Derm Venereol 28, 454, 1948.
51. Aoki, S., Toda, S., Ando, T., and Sugihara, H. Bone marrow stromal cells, preadipocytes, and dermal fibroblasts promote epidermal regeneration in their distinctive fashions. Mol Biol Cell 15, 4647, 2004.
52. El-Ghalbzouri, A., Gibbs, S., Lamme, E., Van Blitterswijk, C.A., and Ponec, M. Effect of fibroblasts on epidermal regeneration. Br J Dermatol 147, 230, 2002.
53. Igarashi, A., Okochi, H., Bradham, D.M., and Grotendorst, G.R. Regulation of connective tissue growth factor gene expression in human skin fibroblasts and during wound repair. Mol Biol Cell 4, 637, 1993.
54. Ninikoski, J., and Hunt, T.K. Measurement of wound oxygen with implanted Silastic tube. Surgery 71, 22, 1972.