Skin and oral mucosa equivalents: Construction and performance

Orthodontics and Craniofacial Research

Volumn 13, Issue 1, 2010, Pages 11-20

  Liu, J ^b   Bian, Z ^b   Kuijpers Jagtman, A M ^a   Von Den Hoff, J W ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b WUHAN UNIVERSITY   (China)

Author keywords

Fibroblasts; Keratinocytes; Oral mucosa; Skin; Tissue engineering

Indexed keywords

TISSUE SCAFFOLD;

ANIMAL; ARTIFICIAL SKIN; EPITHELIUM CELL; HISTOLOGY; HUMAN; MOUTH MUCOSA; REVIEW; SKIN; SKIN TRANSPLANTATION; STEM CELL TRANSPLANTATION; TISSUE ENGINEERING; TRANSPLANTATION;

ANIMALS; EPITHELIAL CELLS; HUMANS; MOUTH MUCOSA; SKIN; SKIN TRANSPLANTATION; SKIN, ARTIFICIAL; STEM CELL TRANSPLANTATION; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 74049154759     PISSN: 16016335     EISSN: 16016343     Source Type: Journal    
DOI: 10.1111/j.1601-6343.2009.01475.x     Document Type: Review

References (94)

1. Presland RB, Jurevic RJ. Making sense of the epithelial barrier: what molecular biology and genetics tell us about the functions of oral mucosal and epidermal tissues. J Dent Educ 2002 66 : 564 574.
2. Prasanna M, Mishra P, Thomas C. Delayed primary closure of the burn wounds. Burns 2004 30 : 169 175.
3. Xiao-Wu W, Herndon DN, Spies M, Sanford AP, Wolf SE. Effects of delayed wound excision and grafting in severely burned children. Arch Surg 2002 137 : 1049 1054.
4. Rosenberg AS, Munttz TI, Maniero TG, Singer A. Cellular basis of skin allograft rejection across a class I major histocompatibility barrier in mice depleted of CD8+ T cells in vivo. J Exp Med 1991 173 : 1463 1471.
5. Fowler EB, Breault LG. Root coverage with an acellular dermal allograft: a three-month case report. J Contemp Dent Pract 2000 1 : 47 59.
6. Rhee PH, Friedman CD, Ridge JA, Kusiak J. The use of processed allograft dermal matrix for intraoral resurfacing: an alternative to split-thickness skin grafts. Arch Otolaryngol Head Neck Surg 1998 124 : 1201 1204.
7. Toft K, Keller GS, Blackwell KE. Ectopic hair growth after flap reconstruction of the head and neck. Arch Facial Plast Surg 2000 2 : 148 150.
8. Vural E, Suen JY. The submental island flap in head and neck reconstruction. Head Neck 2000 22 : 572 578.
9. Tomasek JJ, Gabbiani G, Hinz B, Chaponnier C, Brown RA. Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat Rev Mol Cell Biol 2002 3 : 349 363.
10. Tanaka A, Hatoko M, Tada H, Kuwahara M. An evaluation of functional improvement following surgical corrections of severe burn scar contracture in the axilla. Burns 2003 29 : 153 157.
11. Moore P, Moore M, Blakeney P, Meyer W, Murphy L, Herndon D. Competence and physical impairment of pediatric survivors of burns of more than 80% total body surface area. J Burn Care Rehabil 1996 17 : 547 551.
12. Mølsted K. Treatment outcome in cleft lip and palate: issues and perspectives. Crit Rev Oral Biol Med 1999 10 : 225 239.
13. Ross RB. Growth of the facial skeleton following the Malek repair for unilateral cleft lip and palate. Cleft Palate Craniofac J 1995 32 : 194 198.
14. Wijdeveld MG, Maltha JC, Grupping EM, De Jonge J, Kuijpers-Jagtman AM. A histological study of tissue response to simulated cleft palate surgery at different ages in beagle dogs. Arch Oral Biol 1991 36 : 837 843.
15. Arnold HL Jr., Odom RB, James WD. The skin: basic structure and function. In : James WD, Elston D, Berger T editors. Andrew's Disease of the Skin. San Francisco : Elsevier 1990. pp. 1 13.
16. Squier CA, Kremer MJ. Biology of oral mucosa and esophagus. J Natl Cancer Inst Monogr 2001 29 : 7 15.
17. Squier CA, Finkelstein MW. Oral Mucosa. In : Nanci A editor. Ten Cate's Oral Histology. St. Louis : Mosby 2003. pp. 329 375.
18. Rheinwald JG, Green H. Serial cultivation of strains of human epidermal keratinocytes: the formation of keratinizing colonies from single cells. Cell 1975 6 : 331 343.
19. Krasna M, Planinsek F, Knezevic M, Arnez ZM, Jeras M. Evaluation of a fibrin-based skin substitute prepared in a defined keratinocyte medium. Int J Pharm 2005 291 : 31 7.
20. Sheridan RL, Tompkins RG. Cultured autologous epithelium in patients with burns of ninety percent or more of the body surface. J Trauma 1995 38 : 48 50.
21. Alvarez-Diaz C, Cuenca-Pardo J, Sosa-Serrano A, Juarez-Aguilar E, Marsch-Moreno M, Kuri-Harcuch W. Controlled clinical study of deep partial-thickness burns treated with frozen cultured human allogeneic epidermal sheets. J Burn Care Rehabil 2000 21 : 291 299.
22. Kim BM, Suzuki S, Nishimura Y, Um SC, Morota K, Maruguchi T et al. Cellular artificial skin substitute produced by short period simultaneous culture of fibroblasts and keratinocytes. Br J Plast Surg 1999 52 : 573 578.
23. Kopp J, Jeschke MG, Bach AD, Kneser U, Horch RE. Applied tissue engineering in the closure of severe burns and chronic wounds using cultured human autologous keratinocytes in a natural fibrin matrix. Cell Tissue Bank 2004 5 : 89 96.
24. Horch RE, Bannasch H, Kopp J, Andree C, Stark GB. Cultured human keratinocytes on type I collagen membranes to reconstitute the epidermis. Tissue Eng 2000 6 : 53 67.
25. Wright KA, Nadire KB, Busto P, Tubo R, McPherson JM, Wentworth BM. Alternative delivery of keratinocytes using a polyurethane membrane and the implications for its use in the treatment of full-thickness burn injury. Burns 1998 24 : 7 17.
26. Currie LJ, Martin R, Sharpe JR, James SE. A comparison of keratinocyte cell sprays with and without fibrin glue. Burns 2003 29 : 677 685.
27. Horch RE, Debus M, Wagner G, Stark GB. Single-cell suspensions of cultured human keratinocytes in fibrin-glue reconstitute the epidermis. Cell Transplant 1998 7 : 309 317.
28. Weiss E, Yamaguchi Y, Falabella A, Crane S, Tokuda Y, Falanga V. Un-cross-linked fibrin substrates inhibit keratinocyte spreading and replication: correction with fibronectin and factor XIII cross-linking. J Cell Physiol 1998 174 : 58 65.
29. Mis B, Rolland E, Ronfard V. Combined use of a collagen-based dermal substitute and a fibrin-based cultured epithelium: a step toward a total skin replacement for acute wounds. Burns 2004 30 : 713 719.
30. Ronfard V, Rives JM, Neveux Y, Carsin H, Barrandon Y. Long-term regeneration of human epidermis on third degree burns transplanted with autologous cultured epithelium grown on a fibrin matrix. Transplantation 2000 70 : 1588 1598.
31. Kang MK, Bibb C, Baluda MA, Rey O, Park NH. In vitro replication and differentiation of normal human oral keratinocytes. Exp Cell Res 2000 258 : 288 297.
32. Pomahac B, Svensjo T, Yao F, Brown H, Eriksson E. Tissue engineering of skin. Crit Rev Oral Biol Med 1998 9 : 333 344.
33. Gibbs S, Ponec M. Intrinsic regulation of differentiation markers in human epidermis, hard palate and buccal mucosa. Arch Oral Biol 2000 45 : 149 158.
34. Bodner L, Grossman N. Autologous cultured mucosal graft to cover large intraoral mucosal defects: a clinical study. J Oral Maxillofac Surg 2003 61 : 169 173.
35. Lauer G, Schimming R. Tissue-engineered mucosa graft for reconstruction of the intraoral lining after freeing of the tongue: a clinical and immunohistologic study. J Oral Maxillofac Surg 2001 59 : 169 175. discussion 175-7.
36. Sauerbier S, Gutwald R, Wiedmann-Al-Ahmad M, Lauer G, Schmelzeisen R. Clinical application of tissue-engineered transplants. Part I: mucosa. Clin Oral Implants Res 2006 17 : 625 632.
37. Alonso L, Fuchs E. Stem cells of the skin epithelium. Proc Natl Acad Sci U S A 2003 100 (Suppl 1 11830 11835.
38. Janes SM, Lowell S, Hutter C. Epidermal stem cells. J Pathol 2002 197 : 479 491.
39. Brouard M, Barrandon Y. Controlling skin morphogenesis: hope and despair. Curr Opin Biotechnol 2003 14 : 520 525.
40. Izumi K, Tobita T, Feinberg SE. Isolation of human oral keratinocyte progenitor/stem cells. J Dent Res 2007 86 : 341 346.
41. Bickenbach JR, Chism E. Selection and extended growth of murine epidermal stem cells in culture. Exp Cell Res 1998 244 : 184 195.
42. Dunnwald M, Tomanek-Chalkley A, Alexandrunas D, Fishbaugh J, Bickenbach JR. Isolating a pure population of epidermal stem cells for use in tissue engineering. Exp Dermatol 2001 10 : 45 54.
43. Zhou JX, Jia LW, Yang YJ, Peng S, Cao YJ, Duan EK. Enrichment and characterization of mouse putative epidermal stem cells. Cell Biol Int 2004 28 : 523 529.
44. Ruszczak Z. Effect of collagen matrices on dermal wound healing. Adv Drug Deliv Rev 2003 55 : 1595 1611.
45. Ng KW, Khor HL, Hutmacher DW. In vitro characterization of natural and synthetic dermal matrices cultured with human dermal fibroblasts. Biomaterials 2004 25 : 2807 2818.
46. Yannas IV, Burke JF. Design of an artificial skin. I. Basic design principles. J Biomed Mater Res 1980 14 : 65 81.
47. Yannas IV, Burke JF, Gordon PL, Huang C, Rubenstein RH. Design of an artificial skin. II. Control of chemical composition. J Biomed Mater Res 1980 14 : 107 132.
48. Dantzer E, Braye FM. Reconstructive surgery using an artificial dermis (Integra): results with 39 grafts. Br J Plast Surg 2001 54 : 659 664.
49. Kanitakis J. Clinical evaluation of skin substitutes. Burns 2001 27 : 545 551.
50. Papp A, Harma MA. collagen based dermal substitute and the modified Meek technique in extensive burns. Report of three cases. Burns 2003 29 : 167 171.
51. Jeschke MG, Rose C, Angele P, Fuchtmeier B, Nerlich MN, Bolder U. Development of new reconstructive techniques: use of Integra in combination with fibrin glue and negative-pressure therapy for reconstruction of acute and chronic wounds. Plast Reconstr Surg 2004 113 : 525 530.
52. Palao R, Gomez P, Huguet P. Burned breast reconstructive surgery with Integra dermal regeneration template. Br J Plast Surg 2003 56 : 252 259.
53. Lorenz C, Petracic A, Hohl HP, Wessel L, Waag KL. Early wound closure and early reconstruction. Experience with a dermal substitute in a child with 60 per cent surface area burn. Burns 1997 23 : 505 508.
54. Suzuki S, Kawai K, Ashoori F, Morimoto N, Nishimura Y, Ikada Y. Long-term follow-up study of artificial dermis composed of outer silicone layer and inner collagen sponge. Br J Plast Surg 2000 53 : 659 666.
55. Wainwright DJ. Use of an acellular allograft dermal matrix (AlloDerm) in the management of full-thickness burns. Burns 1995 21 : 243 248.
56. Takami Y, Matsuda T, Yoshitake M, Hanumadass M, Walter RJ. Dispase/detergent treated dermal matrix as a dermal substitute. Burns 1996 22 : 182 190.
57. Tark KC, Chung S, Shin KS, Park BY. Skin flap prefabrication using acellular dermal matrix and cultured keratinocytes in a porcine model. Ann Plast Surg 2000 44 : 392 397.
58. Munster AM, Smith-Meek M, Shalom A. Acellular allograft dermal matrix: immediate or delayed epidermal coverage? Burns 2001 27 : 150 153.
59. Gore DC. Utility of acellular allograft dermis in the care of elderly burn patients. J Surg Res 2005 125 : 37 41.
60. Clark JM, Saffold SH, Israel JM. Decellularized dermal grafting in cleft palate repair. Arch Facial Plast Surg 2003 5 : 40 4. discussion 45.
61. Fowler EB, Breault LG, Rebitski G. Ridge preservation utilizing an acellular dermal allograft and demineralized freeze-dried bone allograft: Part I. A report of 2 cases. J Periodontol 2000 71 : 1353 1359.
62. El Ghalbzouri A, Lamme E, Ponec M. Crucial role of fibroblasts in regulating epidermal morphogenesis. Cell Tissue Res 2002 310 : 189 199.
63. Erdag G, Sheridan RL. Fibroblasts improve performance of cultured composite skin substitutes on athymic mice. Burns 2004 30 : 322 328.
64. Wang HJ, Pieper J, Schotel R, van Blitterswijk CA, Lamme EN. Stimulation of skin repair is dependent on fibroblast source and presence of extracellular matrix. Tissue Eng 2004 10 : 1054 1064.
65. Marston WA, Hanft J, Norwood P, Pollak R. The efficacy and safety of Dermagraft in improving the healing of chronic diabetic foot ulcers: results of a prospective randomized trial. Diabetes Care 2003 26 : 1701 1705.
66. Lamme EN, Van Leeuwen RT, Brandsma K, Van Marle J, Middelkoop E. Higher numbers of autologous fibroblasts in an artificial dermal substitute improve tissue regeneration and modulate scar tissue formation. J Pathol 2000 190 : 595 603.
67. Morimoto N, Saso Y, Tomihata K, Taira T, Takahashi Y, Ohta M et al. Viability and function of autologous and allogeneic fibroblasts seeded in dermal substitutes after implantation. J Surg Res 2005 125 : 56 67.
68. Kubo K, Kuroyanagi Y. Development of a cultured dermal substitute composed of a spongy matrix of hyaluronic acid and atelo-collagen combined with fibroblasts: cryopreservation. Artif Organs 2004 28 : 182 188.
69. Kuroyanagi Y, Kubo K, Matsui H, Kim HJ, Numari S, Mabuchi Y et al. Establishment of banking system for allogeneic cultured dermal substitute. Artif Organs 2004 28 : 13 21.
70. Laning JC, DeLuca JE, Hardin-Young J. Effects of immunoregulatory cytokines on the immunogenic potential of the cellular components of a bilayered living skin equivalent. Tissue Eng 1999 5 : 171 181.
71. Lamme EN, van Leeuwen RT, Jonker A, van Marle J, Middelkoop E. Living skin substitutes: survival and function of fibroblasts seeded in a dermal substitute in experimental wounds. J Invest Dermatol 1998 111 : 989 995.
72. Dai NT, Williamson MR, Khammo N, Adams EF, Coombes AG. Composite cell support membranes based on collagen and polycaprolactone for tissue engineering of skin. Biomaterials 2004 25 : 4263 4271.
73. Kremer M, Lang E, Berger AC. Evaluation of dermal-epidermal skin equivalents ('composite-skin') of human keratinocytes in a collagen- glycosaminoglycan matrix(Integra artificial skin). Br J Plast Surg 2000 53 : 459 465.
74. Yang EK, Seo YK, Youn HH, Lee DH, Park SN, Park JK. Tissue engineered artificial skin composed of dermis and epidermis. Artif Organs 2000 24 : 7 17.
75. Chakrabarty KH, Dawson RA, Harris P, Layton C, Babu M, Gould L et al. Development of autologous human dermal-epidermal composites based on sterilized human allodermis for clinical use. Br J Dermatol 1999 141 : 811 823.
76. El-Ghalbzouri A, Gibbs S, Lamme E, Van Blitterswijk CA, Ponec M. Effect of fibroblasts on epidermal regeneration. Br J Dermatol 2002 147 : 230 243.
77. Herson MR, Mathor MB, Altran S, Capelozzi VL, Ferreira MC. In vitro construction of a potential skin substitute through direct human keratinocyte plating onto decellularized glycerol-preserved allodermis. Artif Organs 2001 25 : 901 906.
78. Caruso DM, Schuh WH, Al-Kasspooles MF, Chen MC, Schiller WR. Cultured composite autografts as coverage for an extensive body surface area burn: case report and review of the technology. Burns 1999 25 : 771 779.
79. Sheridan RL, Morgan JR, Cusick JL, Petras LM, Lydon MM, Tompkins RG. Initial experience with a composite autologous skin substitute. Burns 2001 27 : 421 424.
80. Nanchahal J, Dover R, Otto WR. Allogeneic skin substitutes applied to burns patients. Burns 2002 28 : 254 257.
81. Kinsner A, Lesiak-Cyganowska E, Sladowski D. In vitro reconstruction of full thickness human skin on a composite collagen material. Cell Tissue Bank 2001 2 : 165 171.
82. Gibbs S, van den Hoogenband HM, Kirtschig G, Richters CD, Spiekstra SW, Breetveld M et al. Autologous full-thickness skin substitute for healing chronic wounds. Br J Dermatol 2006 155 : 267 274.
83. Chung JH, Cho KH, Lee DY, Kwon OS, Sung MW, Kim KH et al. Human oral buccal mucosa reconstructed on dermal substrates: a model for oral epithelial differentiation. Arch Dermatol Res 1997 289 : 677 685.
84. Song J, Izumi K, Lanigan T, Feinberg SE. Development and characterization of a canine oral mucosa equivalent in a serum-free environment. J Biomed Mater Res A 2004 71 : 143 153.
85. Izumi K, Feinberg SE, Iida A, Yoshizawa M. Intraoral grafting of an ex vivo produced oral mucosa equivalent: a preliminary report. Int J Oral Maxillofac Surg 2003 32 : 188 197.
86. Cho KH, Ahn HT, Park KC, Chung JH, Kim SW, Sung MW et al. Reconstruction of human hard-palate mucosal epithelium on de-epidermized dermis. J Dermatol Sci 2000 22 : 117 124.
87. Izumi K, Takacs G, Terashi H, Feinberg SE. Ex vivo development of a composite human oral mucosal equivalent. J Oral Maxillofac Surg 1999 57 : 571 577. discussion 577-8.
88. Liu J, Lamme EN, Steegers-Theunissen RP, Krapels IP, Bian Z, Marres H et al. Cleft palate cells can regenerate a palatal mucosa in vitro. J Dent Res 2008 87 : 788 792.
89. Ophof R, van Rheden RE, Von den HJ, Schalkwijk J, Kuijpers-Jagtman AM. Oral keratinocytes cultured on dermal matrices form a mucosa-like tissue. Biomaterials 2002 23 : 3741 3748.
90. Kikuchi Y, Tamai K, Kaneda Y. Cutaneous gene delivery. J Dermatol Sci 2008 50 : 87 98.
91. Goto M, Sawamura D, Ito K, Abe M, Nishie W, Sakai K et al. Fibroblasts show more potential as target cells than keratinocytes in COL7A1 gene therapy of dystrophic epidermolysis bullosa. J Invest Dermatol 2006 126 : 766 772.
92. Mavilio F, Pellegrini G, Ferrari S, Di Nunzio F, Di Iorio E, Recchia A et al. Correction of junctional epidermolysis bullosa by transplantation of genetically modified epidermal stem cells. Nat Med 2006 12 : 1397 1402.
93. Lei P, Ogunade A, Kirkwood KL, Laychock SG, Andreadis ST. Efficient production of bioactive insulin from human epidermal keratinocytes and tissue-engineered skin substitutes: implications for treatment of diabetes. Tissue Eng 2007 13 : 2119 2131.
94. Peroni CN, Cecchi CR, Damiani R, Soares CR, Ribela MT, do Rocio Arkaten R et al. High-level secretion of growth hormone by retrovirally transduced primary human keratinocytes: prospects for an animal model of cutaneous gene therapy. Mol Biotechnol 2006 34 : 239 245.