Current progress of skin tissue engineering: Seed cells, bioscaffolds, and construction strategies
Tóm tắt
The development of cell biology, molecular biology, and material science, has been propelling biomimic tissue-engineered skins to become more sophisticated in scientificity and more simplified in practicality. In order to improve the safety, durability, elasticity, biocompatibility, and clinical efficacy of tissue-engineered skin, several powerful seed cells have already found their application in wound repair, and a variety of bioactive scaff olds have been discovered to influence cell fate in epidermogenesis. These exuberant interests provide insights into advanced construction strategies for complex skin mimics. Based on these exciting developments, a complete full-thickness tissue-engineered skin is likely to be generated.
Tài liệu tham khảo
Shevchenko RV, James SL, James SE. A review of tissue-engineered skin bioconstructs available for skin reconstruction. J R Soc Interface 2010;7:229–58.
Rheinwald JG, Green H. Serial cultivation of strains of human epidermal keratinocytes: The formation of keratinizing colonies from single cells. Cell 1975;6:331–43.
Bottcher-Haberzeth S, Biedermann T, Reichmann E. Tissue engineering of skin. Burns 2010;36:450–60.
Abbas O, Mahalingam M. Epidermal stem cells: Practical perspectives and potential uses. Br J Dermatol 2009;161:228–36.
Wood FM, Kolybaba ML, Allen P. The use of cultured epithelial autograft in the treatment of major burn wounds: Eleven years of clinical experience. Burns 2006;32:538–44.
Clugston PA, Snelling CF, Macdonald IB, Maledy HL, Boyle JC, Germann E, et al. Cultured epithelial autografts: Three years of clinical experience with eighteen patients. J Burn Care Rehabil 1991;12:533-9.
Lootens L, Brusselaers N, Beele H, Monstrey S. Keratinocytes in the treatment of severe burn injury: An update. Int Wound J 2013;10:6–12.
Cuono C, Langdon R, McGuire J. Use of cultured epidermal autografts and dermal allografts as skin replacement after burn injury. Lancet 1986;1:1123–4.
Butler CE, Orgill DP. Simultaneous in vivo regeneration of neodermis, epidermis, and basement membrane. Adv Biochem Eng Biotechnol 2005;94:23–41.
Duan H, Feng B, Guo X, Wang J, Zhao L, Zhou G, et al. Engineering of epidermis skin grafts using electrospun nanofibrous gelatin/ polycaprolactone membranes. Int J Nanomedicine 2013;8:2077–84.
Currie LJ, Sharpe JR, Martin R. The use of fibrin glue in skin grafts and tissue-engineered skin replacements: A review. Plast Reconstr Surg 2001;108:1713–26.
Howling GI, Dettmar PW, Goddard PA, Hampson FC, Dornish M, Wood EJ. The effect of chitin and chitosan on the proliferation of human skin fibroblasts and keratinocytes in vitro. Biomaterials 2001;22:2959–66.
Kao B, Kadomatsu K, Hosaka Y. Construction of synthetic dermis and skin based on a self-assembled peptide hydrogel scaffold. Tissue Eng Part A 2009;15:2385–96.
Blackwood KA, McKean R, Canton I, Freeman CO, Franklin KL, Cole D, et al. Development of biodegradable electrospun scaffolds for dermal replacement. Biomaterials 2008;29:3091–104.
Sarkar SD, Farrugia BL, Dargaville TR, Dhara S. Chitosan-collagen scaffolds with nano/microfibrous architecture for skin tissue engineering. J Biomed Mater Res A 2013.
Sun T, Jackson S, Haycock JW, MacNeil S. Culture of skin cells in 3D rather than 2D improves their ability to survive exposure to cytotoxic agents. J Biotechnol 2006;122:372–81.
Sun T, Mai S, Norton D, Haycock JW, Ryan AJ, MacNeil S. Self-organization of skin cells in three-dimensional electrospun polystyrene scaffolds. Tissue Eng 2005;11:1023–33.
el-Ghalbzouri A, Gibbs S, Lamme E, Van Blitterswijk CA, Ponec M. Effect of fibroblasts on epidermal regeneration. Br J Dermatol 2002;147:230–43.
Sonnemann KJ, Bement WM. Wound repair: Toward understanding and integration of single-cell and multicellular wound responses. Annu Rev Cell Dev Biol 2011;27:237–63.
Blanpain C. Stem cells: Skin regeneration and repair. Nature 2010;464:686–7.
Ikuta S, Sekino N, Hara T, Saito Y, Chida K. Mouse epidermal keratinocytes in three-dimensional organotypic coculture with dermal fibroblasts form a stratified sheet resembling skin. Biosci Biotechnol Biochem 2006;70:2669–75.
Zhang CP, Fu XB. Therapeutic potential of stem cells in skin repair and regeneration. Chin J Traumatol 2008;11:209–21.
Fernandes KJ, McKenzie IA, Mill P, Smith KM, Akhavan M, Barnabe-Heider F, et al. A dermal niche for multipotent adult skin-derived precursor cells. Nat Cell Biol 2004;6:1082–93.
Ito M, Liu Y, Yang Z, Nguyen J, Liang F, Morris RJ, et al. Stem cells in the hair follicle bulge contribute to wound repair but not to homeostasis of the epidermis. Nat Med 2005;11:1351–4.
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.
Lei XH, Ning LN, Cao YJ, Liu S, Zhang SB, Qiu ZF, et al. NASA-approved rotary bioreactor enhances proliferation of human epidermal stem cells and supports formation of 3D epidermis-like structure. PloS One 2011;6:e26603.
Stenn KS, Cotsarelis G Bioengineering the hair follicle: Fringe benefits of stem cell technology. Curr Opin Biotechnol 2005;16:493–7.
Gagnon V, Larouche D, Parenteau-Bareil R, Gingras M, Germain L, Berthod F Hair follicles guide nerve migration in vitro and in vivo in tissue-engineered skin. J Invest Dermatol 2011;131:1375–8.
Rehder J, Souto LR, Issa CM, Puzzi MB. Model of human epidermis reconstructed in vitro with keratinocytes and melanocytes on dead de-epidermized human dermis. Sao Paulo Med J 2004;122:22–5.
Liu Y, Suwa F, Wang X, Takemura A, Fang YR, Li Y, et al. Reconstruction of a tissue-engineered skin containing melanocytes. Cell Biol Int 2007;31:985–90.
Hachiya A, Sriwiriyanont P, Kaiho E, Kitahara T, Takema Y, Tsuboi R. An in vivo mouse model of human skin substitute containing spontaneously sorted melanocytes demonstrates physiological changes after UVB irradiation. J Invest Dermatol 2005;125:364–72.
Metallo CM, Ji L, de Pablo JJ, Palecek SP. Retinoic acid and bone morphogenetic protein signaling synergize to efficiently direct epithelial differentiation of human embryonic stem cells. Stem Cells 2008;26:372–80.
Aberdam E, Barak E, Rouleau M, de LaForest S, Berrih-Aknin S, Suter DM, et al. A pure population of ectodermal cells derived from human embryonic stem cells. Stem Cells 2008;26:440–4.
Inanc B, Elcin AE, Unsal E, Balos K, Parlar A, Elcin YM. Differentiation of human embryonic stem cells on periodontal ligament fibroblasts in vitro. Artif Organs 2008;32:100–9.
Metallo CM, Azarin SM, Moses LE, Ji L, de Pablo JJ, Palecek SP. Human embryonic stem cell-derived keratinocytes exhibit an epidermal transcription program and undergo epithelial morphogenesis in engineered tissue constructs. Tissue Eng Part A 2010;16:213–23.
Hewitt KJ, Shamis Y, Carlson MW, Aberdam E, Aberdam D, Garlick JA. Three-dimensional epithelial tissues generated from human embryonic stem cells. Tissue Eng Part A 2009;15:3417–26.
Guenou H, Nissan X, Larcher F, Feteira J, Lemaitre G, Saidani M, et al. Human embryonic stem-cell derivatives for full reconstruction of the pluristratified epidermis: A preclinical study. Lancet 2009;374:1745–53.
Han YF, Tao R, Sun TJ, Chai JK, Xu G, Liu J. Advances and opportunities for stem cell research in skin tissue engineering. Eur Rev Med Pharmacol Sci 2012;16:1873–7.
Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006;126:663–76.
Qi H, Pei D. The magic of four: Induction of pluripotent stem cells from somatic cells by Oct4, Sox2, Myc and Klf4. Cell Res 2007;17:578–80.
Bilousova G, Chen J, Roop DR. Differentiation of mouse induced pluripotent stem cells into a multipotent keratinocyte lineage. J Invest Dermatol 2011;131:857–64.
Sakurai M, Hayashi R, Kageyama T, Yamato M, Nishida K. Induction of putative stratified epithelial progenitor cells in vitro from mouse-induced pluripotent stem cells. J Artif Organs 2011;14:58–66.
Tolar J, Xia L, Riddle MJ, Lees CJ, Eide CR, McElmurry RT, et al. Induced pluripotent stem cells from individuals with recessive dystrophic epidermolysis bullosa. J Invest Dermatol 2011;131:848–56.
Okita K, Nakagawa M, Hyenjong H, Ichisaka T, Yamanaka S. Generation of mouse induced pluripotent stem cells without viral vectors. Science 2008;322:949–53.
Uitto J. Regenerative medicine for skin diseases: iPS cells to the rescue. J Invest Dermatol 2011;131:812–4.
Vogel G. Stem cells. Diseases in a dish take off. Science 2010;330:1172–3.
Badylak SF, Taylor D, Uygun K. Whole-organ tissue engineering: Decellularization and recellularization of three-dimensional matrix scaffolds. Annu Rev Biomed Eng 2011;13:27–53.
Hodgkinson T, Bayat A. Dermal substitute-assisted healing: Enhancing stem cell therapy with novel biomaterial design. Arch Dermatol Res 2011;303:301–15.
Wu Y, Chen L, Scott PG, Tredget EE. Mesenchymal stem cells enhance wound healing through differentiation and angiogenesis. Stem Cells 2007;25:2648–59.
Li H, Fu X, Ouyang Y, Cai C, Wang J, Sun T. Adult bone-marrow-derived mesenchymal stem cells contribute to wound healing of skin appendages. Cell Tissue Res 2006;326:725–36.
Caplan AI. Why are MSCs therapeutic? New data: New insight. J Pathol 2009;217:318–24.
Rasmusson I, Le Blanc K, Sundberg B, Ringden O. Mesenchymal stem cells stimulate antibody secretion in human B cells. Scand J Immunol 2007;65:336–43.
Schneider RK, Neuss S, Stainforth R, Laddach N, Bovi M, Knuechel R, et al. Three-dimensional epidermis-like growth of human mesenchymal stem cells on dermal equivalents: Contribution to tissue organization by adaptation of myofibroblastic phenotype and function. Differentiation 2008;76:156–67.
Schneider RK, Puellen A, Kramann R, Raupach K, Bornemann J, Knuechel R, et al. The osteogenic differentiation of adult bone marrow and perinatal umbilical mesenchymal stem cells and matrix remodelling in three-dimensional collagen scaffolds. Biomaterials 2010;31:467–80.
Liu P, Deng Z, Han S, Liu T, Wen N, Lu W, et al. Tissue-engineered skin containing mesenchymal stem cells improves burn wounds. Artif Organs 2008;32:925–31.
Huang SP, Hsu CC, Chang SC, Wang CH, Deng SC, Dai NT, et al. Adipose-derived stem cells seeded on acellular dermal matrix grafts enhance wound healing in a murine model of a full-thickness defect. Ann Plast Surg 2012;69:656–62.
Liu S, Zhang H, Zhang X, Lu W, Huang X, Xie H, et al. Synergistic angiogenesis promoting effects of extracellular matrix scaffolds and adipose-derived stem cells during wound repair. Tissue Eng Part A 2011;17:725–39.
Hendrickx B, Vranckx JJ, Luttun A. Cell-based vascularization strategies for skin tissue engineering. Tissue Eng Part B Rev 2011;17:13–24.
Zhang X, Yang J, Li Y, Liu S, Long K, Zhao Q, et al. Functional neovascularization in tissue engineering with porcine acellular dermal matrix and human umbilical vein endothelial cells. Tissue Eng Part C Methods 2011;17:423–33.
Hudon V, Berthod F, Black AF, Damour O, Germain L, Auger FA. A tissue-engineered endothelialized dermis to study the modulation of angiogenic and angiostatic molecules on capillary-like tube formation in vitro. Br J Dermatol 2003;148:1094–104.
Kunz-Schughart LA, Schroeder JA, Wondrak M, van Rey F, Lehle K, Hofstaedter F, et al. Potential of fibroblasts to regulate the formation of three-dimensional vessel-like structures from endothelial cells in vitro. Am J Physiol Cell Physiol 2006;290:C1385–98.
Liu Y, Luo H, Wang X, Takemura A, Fang YR, Jin Y, et al. In vitro construction of scaffold-free bilayered tissue-engineered skin containing capillary networks. Biomed Res Int 2013;2013:561410.
Kesting MR, Wolff KD, Hohlweg-Majert B, Steinstraesser L. The role of allogenic amniotic membrane in burn treatment. J Burn Care Res 2008;29:907–16.
Shimmura S, Shimazaki J, Ohashi Y, Tsubota K. Antiinflammatory effects of amniotic membrane transplantation in ocular surface disorders. Cornea 2001;20:408–13.
Li H, Chu Y, Zhang Z, Zhang G, Jiang L, Wu H, et al. Construction of bilayered tissue-engineered skin with human 71 amniotic mesenchymal cells and human amniotic epithelial cells. Artif Organs 2012;36:911–9.
Hartmann-Fritsch F, Hosper N, Luginbuhl J, Biedermann T, Reichmann E, Meuli M. Human amniotic fluid derived cells can competently substitute dermal fibroblasts in a tissue-engineered dermo-epidermal skin analog. Pediatr Surg Int 2013;29:61–9.
Ruszczak Z. Effect of collagen matrices on dermal wound healing. Adv Drug Deliv Rev 2003;55:1595–611.
Shin H, Jo S, Mikos AG. Biomimetic materials for tissue engineering. Biomaterials 2003;24:4353-64.
Nam K, Kimura T, Funamoto S, Kishida A. Preparation of a collagen/polymer hybrid gel designed for tissue membranes. Part I: Controlling the polymer-collagen cross-linking process using an ethanol/water co-solvent. Acta Biomater 2010;6:403–8.
Weadock KS, Miller EJ, Keuffel EL, Dunn MG. Effect of physical crosslinking methods on collagen-fiber durability in proteolytic solutions. J Biomed Mater Res 1996;32:221–6.
Wang HM, Chou YT, Wen ZH, Wang ZR, Chen CH, Ho ML. Novel biodegradable porous scaffold applied to skin regeneration. PloS One 2013;8:e56330.
Faraj KA, van Kuppevelt TH, Daamen WF Construction of collagen scaffolds that mimic the three-dimensional architecture of specific tissues. Tissue Eng 2007;13:2387–94.
Rnjak-Kovacina J, Wise SG, Li Z, Maitz PK, Young CJ, Wang Y, et al. Electrospun synthetic human elastin: Collagen composite scaffolds for dermal tissue engineering. Acta Biomater 2012;8:3714–22.
Nillesen ST, Geutjes PJ, Wismans R, Schalkwijk J, Daamen WF, van Kuppevelt TH. Increased angiogenesis and blood vessel maturation in acellular collagen-heparin scaffolds containing both FGF2 and VEGF. Biomaterials 2007;28:1123–31.
Lynn AK, Yannas IV, Bonfield W. Antigenicity and immunogenicity of collagen. J Biomed Mater Res B Appl Biomater 2004;71:343–54.
Lee CH, Singla A, Lee Y. Biomedical applications of collagen. Int J Pharm 2001;221:1–22.
Khor HL, Ng KW, Schantz JT, Phan TT, Lim TC, Teoh SH, et al. Poly (?-caprolactone) films as a potential substrate for tissue engineering an epidermal equivalent. Mater Sci Eng C 2002;20:71–5.
Sun T, Haycock J, MacNeil S. In situ image analysis of interactions between normal human keratinocytes and fibroblasts cultured in three-dimensional fibrin gels. Biomaterials 2006;27:3459–65.
Wang TW, Sun JS, Wu HC, Tsuang YH, Wang WH, Lin FH. The effect of gelatin-chondroitin sulfate-hyaluronic acid skin substitute on wound healing in SCID mice. Biomaterials 2006;27:5689–97.
Lee SB, Kim YH, Chong MS, Hong SH, Lee YM. Study of gelatin-containing artificial skin V: Fabrication of gelatin scaffolds using a salt-leaching method. Biomaterials 2005;26:1961–8.
Meana A, Iglesias J, Del Rio M, Larcher F, Madrigal B, Fresno M, et al. Large surface of cultured human epithelium obtained on a dermal matrix based on live fibroblast-containing fibrin gels. Burns 1998;24:621–30.
Hodgkinson T, Bayat A. Dermal substitute-assisted healing: Enhancing stem cell therapy with novel biomaterial design. Arch Dermatol Res 2011;303:301–15.
Chun YS, Verma K, Rosen H, Lipsitz S, Morris D, Kenney P, et al. Implant-based breast reconstruction using acellular dermal matrix and the risk of postoperative complications. Plast Reconstr Surg 2010;125:429–36.
Askari M, Cohen MJ, Grossman PH, Kulber DA. The use of acellular dermal matrix in release of burn contracture scars in the hand. Plast Reconstr Surg 2011;127:1593–9.
Ge L, Zheng S, Wei H. Comparison of histological structure and biocompatibility between human acellular dermal matrix (ADM) and porcine ADM. Burns 2009;35:46–50.
Derwin KA, Badylak SF, Steinmann SP, Iannotti JP. Extracellular matrix scaffold devices for rotator cuff repair. J Shoulder Elbow Surg 2010;19:467–76.
Reing JE, Zhang L, Myers-Irvin J, Cordero KE, Freytes DO, Heber-Katz E, et al. Degradation products of extracellular matrix affect cell migration and proliferation. Tissue Eng Part A 2009;15:605–14.
Chen RN, Ho HO, Tsai YT, Sheu MT. Process development of an acellular dermal matrix (ADM) for biomedical applications. Biomaterials 2004;25:2679–86.
Callcut R, Schurr M, Sloan M, Faucher L. Clinical experience with Alloderm: A one-staged composite dermal/epidermal replacement utilizing processed cadaver dermis and thin autografts. Burns 2006;32:583–8.
Zhang X, Deng Z, Wang H, Yang Z, Guo W, Li Y, et al. Expansion and delivery of human fibroblasts on micronized acellular dermal matrix for skin regeneration. Biomaterials 2009;30:2666–74.
Sanders J, Stiles C, Hayes C. Tissue response to single-polymer fibers of varying diameters: Evaluation of fibrous encapsulation and macrophage density. J Biomed Mater Res 2000;52:231–7.
Dai W, Kawazoe N, Lin X, Dong J, Chen G. The influence of structural design of PLGA/collagen hybrid scaffolds in cartilage tissue engineering. Biomaterials 2010;31:2141–52.
Chen X, Qi YY, Wang LL, Yin Z, Yin GL, Zou XH, et al. Ligament regeneration using a knitted silk scaffold combined with collagen matrix. Biomaterials 2008;29:3683–92.
Chen G, Sato T, Ohgushi H, Ushida T, Tateishi T, Tanaka J. Culturing of skin fibroblasts in a thin PLGA-collagen hybrid mesh. Biomaterials 2005;26:2559–66.
Lin HY, Kuo YJ, Chang SH, Ni TS. Characterization of electrospun nanofiber matrices made of collagen blends as potential skin substitutes. Biomed Mater 2013;8:025009.
Cui W, Zhu X, Yang Y, Li X, Jin Y. Evaluation of electrospun fibrous scaffolds of poly (dl-lactide) and poly (ethylene glycol) for skin tissue engineering. Mater Sci Eng C 2009;29:1869–76.
Ma G, Yang D, Wang K, Han J, Ding S, Song G, et al. Organic?soluble chitosan/polyhydroxybutyrate ultrafine fibers as skin regeneration prepared by electrospinning. J Appl Polym Sci 2010;118:3619–24.
Lammers G, Tjabringa GS, Schalkwijk J, Daamen WF, van Kuppevelt TH. A molecularly defined array based on native fibrillar collagen for the assessment of skin tissue engineering biomaterials. Biomaterials 2009;30:6213–20.
Yliperttula M, Chung BG, Navaladi A, Manbachi A, Urtti A. High-throughput screening of cell responses to biomaterials. Eur J Pharm Sci 2008;35:151–60.
Kennedy SB, Washburn NR, Simon CG Jr, Amis EJ. Combinatorial screen of the effect of surface energy on fibronectin-mediated osteoblast adhesion, spreading and proliferation. Biomaterials 2006;27:3817–24.
MacNeil S. Progress and opportunities for tissue-engineered skin. Nature 2007;445:874–80.
Navarro FA, Stoner ML, Park CS, Huertas JC, Lee HB, Wood FM, et al. Sprayed keratinocyte suspensions accelerate 72 epidermal coverage in a porcine microwound model. J Burn Care Rehabil 2000;21:513–8.
Haddow DB, Steele DA, Short RD, Dawson RA, Macneil S. Plasma-polymerized surfaces for culture of human keratinocytes and transfer of cells to an in vitro wound-bed model. J Biomed Mater Res A 2003;64:80–7.
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.
Tausche AK, Skaria M, Bohlen L, Liebold K, Hafner J, Friedlein H, et al. An autologous epidermal equivalent tissue-engineered from follicular outer root sheath keratinocytes is as effective as split-thickness skin autograft in recalcitrant vascular leg ulcers. Wound Repair Regen 2003;11:248–52.
Vaillant L. Treatment of venous leg ulcers with Epibase. A prospective study. Preliminary results. Ann Dermatol Venereol 2002;129:1245–6.
Heimbach DM. A nonuser’s questions about cultured epidermal autograft. J Burn Care Rehabil 1992;13:127–9.
Wainwright D. Use of an acellular allograft dermal matrix (AlloDerm) in the management of full-thickness burns. Burns 1995;21:243-8.
Bond JL, Dopirak RM, Higgins J, Burns J, Snyder SJ. Arthroscopic replacement of massive, irreparable rotator cuff tears using a GraftJacket allograft: Technique and preliminary results. Arthroscopy 2008;24:403–9 e1.
Ryssel H, Gazyakan E, Germann G, Öhlbauer M. The use of MatriDerm® in early excision and simultaneous autologous skin grafting in burns-A pilot study. Burns 2008;34:93–7.
Heimbach DM, Warden GD, Luterman A, Jordan MH, Ozobia N, Ryan CM, et al. Multicenter postapproval clinical trial of Integra dermal regeneration template for burn treatment. J Burn Care Rehabil 2003;24:42–8.
Feldman DL, Rogers A, Karpinski RH. A prospective trial comparing Biobrane, Duoderm and xeroform for skin graft donor sites. Surg Gynecol Obstet 1991;173:1–5.
Gravante G, Delogu D, Giordan N, Morano G, Montone A, Esposito G. The use of Hyalomatrix PA in the treatment of deep partial-thickness burns. J Burn Care Res 2007;28:269–74.
Gentzkow GD, Iwasaki SD, Hershon KS, Mengel M, Prendergast JJ, Ricotta JJ, et al. Use of dermagraft, a cultured human dermis, to treat diabetic foot ulcers. Diabetes Care 1996;19:350–4.
Noordenbos J, Dore C, Hansbrough JF. Safety and efficacy of TransCyte for the treatment of partial-thickness burns. J Burn Care Rehabil 1999;20:275–81.
Falanga V, Sabolinski M. A bilayered living skin construct (APLIGRAF) accelerates complete closure of hard-to-heal venous ulcers. Wound Repair Regen 1999;7:201–7.
El Ghalbzouri A, Commandeur S, Rietveld MH, Mulder AA, Willemze R. Replacement of animal-derived collagen matrix by human fibroblast-derived dermal matrix for human skin equivalent products. Biomaterials 2009;30:71–8.
Dong R, Liu X, Liu Y, Deng Z, Nie X, Wang X, et al. Enrichment of epidermal stem cells by rapid adherence and analysis of the reciprocal interaction of epidermal stem cells with neighboring cells using an organotypic system. Cell Biol Int 2007;31:733–40.
Aoki S, Takezawa T, Uchihashi K, Sugihara H, Toda S. Non-skin mesenchymal cell types support epidermal regeneration in a mesenchymal stem cell or myofibroblast phenotype-independent manner. Pathol Int 2009;59:368–75.
Nie X, Cai JK, Yang HM, Xiao HA, Wang JH, Wen N, et al. Successful application of tissue-engineered skin to refractory ulcers. Clin Exp Dermatol 2007;32:699–701.
Martinez-Santamaria L, Guerrero-Aspizua S, Del Rio M. Skin bioengineering: Preclinical and clinical applications. Actas Dermosifiliogr 2012;103:5–11.
Mahjour SB, Ghaffarpasand F, Wang H. Hair follicle regeneration in skin grafts: Current concepts and future perspectives. Tissue Eng Part B Rev 2012;18:15–23.
Blais M, Grenier M, Berthod F. Improvement of nerve regeneration in tissue-engineered skin enriched with schwann cells. J Invest Dermatol 2009;129:2895–900.
Monfort A, Soriano-Navarro M, Garcia-Verdugo JM, Izeta A. Production of human tissue-engineered skin trilayer on a plasma-based hypodermis. J Tissue Eng Regen Med 2013;7:479–90.
Liu F, Luo XS, Shen HY, Dong JS, Yang J. Using human hair follicle-derived keratinocytes and melanocytes for constructing pigmented tissue-engineered skin. Skin Res Technol 2011;17:373–9.
Peng LH, Mao ZY, Qi XT, Chen X, Li N, Tabata Y, et al. Transplantation of bone-marrow-derived mesenchymal and epidermal stem cells contribute to wound healing with different regenerative features. Cell Tissue Res 2013;352:573–83.
Altman AM, Matthias N, Yan Y, Song YH, Bai X, Chiu ES, et al. Dermal matrix as a carrier for in vivo delivery of human adipose-derived stem cells. Biomaterials 2008;29:1431–42.
Lu W, Yu J, Zhang Y, Ji K, Zhou Y, Li Y, et al. Mixture of fibroblasts and adipose tissue-derived stem cells can improve epidermal morphogenesis of tissue-engineered skin. Cells Tissues Organs 2012;195:197–206.
Griffiths M, Ojeh N, Livingstone R, Price R, Navsaria H. Survival of Apligraf in acute human wounds. Tissue Eng 2004;10:1180–95.