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Skin Cell Cultures and Skin Engineering

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Regenerative Medicine Procedures for Aesthetic Physicians
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Abstract

This chapter is focused on skin regeneration with cultured cells and bioengineered skin substitutes. Different kinds of multipotent stem cells can be found in hair and skin tissues. Cell culture is a well-established research tool in biology and medicine. Several cell culture techniques have been developed in order to obtain different cell types. Different culture techniques will be discussed (use of proteolytic enzymes, 3D cultures, and automatic bioprocessing). Several skin regeneration approaches will be described. In the field of aesthetic medicine, the injection of autologous cultured cells seems to be a good method to restore aging skin. Nevertheless its application is far from being widespread. The challenge of current bioengineering efforts is to generate functional organ systems from dissociated cells that have been expanded under defined tissue culture conditions. Tissue engineering is emerging as a significant potential solution for tissue and organ failure. Clinical applications, efficacy and safety, and trends and limitations of the current techniques will also be discussed. Even though there is still a long way to go, the rise of cell culture and tissue engineering is providing powerful tools for regenerative medicine evolution. Further large-scale and rigorous studies with long-term follow-up should be performed to assess the safety of cell culture and skin substitutes. Great improvements have been made in this field, and now the challenge is its application to routine clinical practice.

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References

  1. Freshney RI. Culture of animal cells: a manual of basic technique and specialized applications. Wiley-Blackwell: Hoboken, NJ; 2016.

    Google Scholar 

  2. Sugiyama-Nakagiri Y, Fujimura T, Moriwaki S. Induction of skin-derived precursor cells from human induced pluripotent stem cells. PLoS One. 2016;11:e0168451. https://doi.org/10.1371/journal.pone.0168451.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Tavakolpour S, Daneshpazhooh M, Mahmoudi H. Skin cancer: genetics, immunology, treatments, and psychological care. In: Mehdipour P, editor. Cancer genetics and psychotherapy. Cham: Springer; 2017. https://doi.org/10.1007/978-3-319-64550-6_18.

    Chapter  Google Scholar 

  4. Choi M, Lee C. Immortalization of primary keratinocytes and its application to skin research. Biomol Ther (Seoul). 2015;23:391–9. https://doi.org/10.4062/biomolther.2015.038.

    Article  CAS  Google Scholar 

  5. Rheinwald JG, Green H. Serial cultivation of strains of human epidermal keratinocytes: the formation of keratinizing colonies from single cells. Cell. 1975;6:331–44.

    Article  CAS  PubMed  Google Scholar 

  6. Rheinwald JG, Green H. Epidermal growth factor and the multiplication of cultured human epidermal keratinocytes. Nature. 1977;265:421–4.

    Article  CAS  PubMed  Google Scholar 

  7. O’Connor N, Mulliken JB, Banks-Schlegel S, Kehinde O, Green H. Grafting of burns with cultured epithelium prepared from autologous epidermal cells. Lancet. 1981;1:75–8.

    Article  Google Scholar 

  8. Li A, Simmons PJ, Kaur P. Identification and isolation of candidate human keratinocyte stem cells based on cell surface phenotype. Proc Natl Acad Sci U S A. 1998;95:3902–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Webb A, Li A, Kaur P. Location and phenotype of human adult keratinocyte stem cells of the skin. Differentiation. 2004;72:387–95. https://doi.org/10.1111/j.1432-0436.2004.07208005.x.

    Article  PubMed  Google Scholar 

  10. Limat A, Mauri D, Hunziker T. Successful treatment of chronic leg ulcers with epidermal equivalents generated from cultured autologous outer root sheath cells. J Invest Dermatol. 1996;107:128–35.

    Article  CAS  PubMed  Google Scholar 

  11. Limat A, French LE, Blal L, Saurat JH, Hunziker T, Salomon D. Organotypic cultures of autologous hair follicle keratinocytes for the treatment of recurrent leg ulcers. J Am Acad Dermatol. 2003;48:207–14. https://doi.org/10.1067/mjd.2003.69.

    Article  PubMed  Google Scholar 

  12. Ohyama M, Terunuma A, Tock CL, Radonovich MF, Pise-Masison CA, Hopping SB, et al. Characterization and isolation of stem cell-enriched human hair follicle bulge cells. J Clin Invest. 2006;116:249–60. https://doi.org/10.1172/JCI26043.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Ohyama M, William J. Cunliffe scientific awards. Advances in the study of stem-cell-enriched hair follicle bulge cells: a review featuring characterization and isolation of human bulge cells. Dermatology. 2007;214:342–51. https://doi.org/10.1159/000100889.

    Article  PubMed  Google Scholar 

  14. Biedermann T, Pontiggia L, Böttcher-Haberzeth S, Tharakan S, Braziulis E, Schiestl C, et al. Human eccrine sweat gland cells can reconstitute a stratified epidermis. J Invest Dermatol. 2010;130(8):1996–2009. https://doi.org/10.1038/jid.2010.83.

    Article  CAS  PubMed  Google Scholar 

  15. Hill R. Skin regeneration symposium Cambridge. Regen Med. 2016;11:443–57. https://doi.org/10.2217/rme-2016-0062.

    Article  CAS  PubMed  Google Scholar 

  16. Penna V, Lipay MV, Duailibi M, Duailibi SE. The likely role of proteolytic enzymes in unwanted differentiation of stem cells in culture. Future Sci OA. 2015;1:FSO28. https://doi.org/10.4155/fso.15.26.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Maniotis AJ, Chen CS, Ingber DE. Demonstration of mechanical connections between integrins, cytoskeletal filaments, and nucleoplasm that stabilize nuclear structure. Proc Natl Acad Sci U S A. 1997;94:849–54.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Lelièvre SA, Bissell MJ. Communication between the cell membrane and the nucleus: role of protein compartmentalization. J Cell Biochem Suppl. 1998;30-31:250–63.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P. Molecular biology of the cell. In: Ltda AMS, editor. Cell junctions, cell adhesion, and the extracellular matrix. 3rd ed. Brazil: Rio Grande do Sul; 2002. p. 949–1010.

    Google Scholar 

  20. DeMali KA, Sun X, Bui GA. Force transmission at cell–cell and cell–matrix adhesions. Biochemistry. 2014;53:7706–17. https://doi.org/10.1021/bi501181p.

    Article  CAS  PubMed  Google Scholar 

  21. Faulk DM, Johnson SA, Zhang L, Badylak SF. Role of the extracellular matrix in whole organ engineering. J Cell Physiol. 2014;229:984–9. https://doi.org/10.1002/jcp.24532.

    Article  CAS  PubMed  Google Scholar 

  22. Spencer VA, Xu R, Bissell MJ. Gene expression in the third dimension: the ECM-nucleus connection. J Mammary Gland Biol Neoplasia. 2010;15:65–71. https://doi.org/10.1007/s10911-010-9163-3.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Ruszczak Z. Effect of collagen matrices on dermal wound healing. Adv Drug Deliv Rev. 2003;55:1595–611.

    Article  CAS  PubMed  Google Scholar 

  24. Zhou H, You C, Wang X, Jin R, Wu P, Li Q, et al. The progress and challenges for dermal regeneration in tissue engineering. J Biomed Mater Res A. 2017;105:1208–18. https://doi.org/10.1002/jbm.a.35996.

    Article  CAS  PubMed  Google Scholar 

  25. Rolfe KJ, Grobbelaar AO. A review of fetal scarless healing. ISRN Dermatol. 2012;2012:698034. https://doi.org/10.5402/2012/698034.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Böttcher-Haberzeth S, Biedermann T, Reichmann E. Tissue engineering of skin. Burns. 2010;36:450–60. https://doi.org/10.1016/j.burns.2009.08.016.

    Article  PubMed  Google Scholar 

  27. Aoki S, Toda S, Ando T, Sugihara H. Bone marrow stromal cells, pre-adipocytes, and dermal fibroblasts promote epidermal regeneration in their distinctive fashions. Mol Biol Cell. 2004;15:4647–57.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Chang HY, Chi JT, Dudoit S, Bondre C, van de Rijn M, Botstein D, et al. Diversity, topographic differentiation, and positional memory in human fibroblasts. Proc Natl Acad Sci U S A. 2002;99:12877–82. https://doi.org/10.1073/pnas.162488599.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Wong T, McGrath JA, Navsaria H. The role of fibroblasts in tissue engineering and regeneration. Br J Dermatol. 2007;156:1149–55. https://doi.org/10.1111/j.1365-2133.2007.07914.x.

    Article  CAS  PubMed  Google Scholar 

  30. Igarashi A, Okochi H, Bradham DM, Grotendorst GR. Regulation of connective tissue growth factor gene expression in human skin fibroblasts and during wound repair. Mol Biol Cell. 1993;4:637–45.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Werner S, Smola H. Paracrine regulation of keratinocyte proliferation and differentiation. Trends Cell Biol. 2001;11:143–6.

    Article  CAS  PubMed  Google Scholar 

  32. 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.

    Article  CAS  PubMed  Google Scholar 

  33. Trompezinski S, Berthier-Vergnes O, Denis A, Schmitt D, Viac J. Comparative expression of vascular endothelial growth factor family members, VEGF-B, -C and -D by normal human keratinocytes and fibroblasts. Exp Dermatol. 2004;13:98–105. https://doi.org/10.1111/j.0906-6705.2004.00137.x.

    Article  CAS  PubMed  Google Scholar 

  34. Rendl M, Polak L, Fuchs E. BMP signaling in dermal papilla cells is required for their hair follicle-inductive properties. Genes Dev. 2008;22:543–57.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Langan EA, Philpott MP, Kloepper JE, Paus R. Human hair follicle organ culture: theory, application and perspectives. Exp Dermatol. 2015;24:903–11. https://doi.org/10.1111/exd.12836.

    Article  PubMed  Google Scholar 

  36. Kumar A, Mohanty S, Nandy SB, Gupta S, Khaitan BK, Sharma S, et al. Hair & skin derived progenitor cells: in search of a candidate cell for regenerative medicine. Indian J Med Res. 2016;143:175–83. https://doi.org/10.4103/0971-5916.180205.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Blanpain C, Fuchs E. Epidermal stem cells of the skin. Annu Rev Cell Dev Biol. 2006;22:339–73.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Lee B, Dai X. Transcriptional control of epidermal stem cells. In: Hime G, Abud H, editors. Transcriptional and translational regulation of stem cells. Advances in experimental medicine and biology, vol. vol. 786. Dordrecht: Springer; 2013. https://doi.org/10.1007/978-94-007-6621-1_9.

    Chapter  Google Scholar 

  39. Ito M, Yang Z, Andl T, Cui C, Kim N, Millar SE, et al. Wnt-dependent de novo hair follicle regeneration in adult mouse skin after wounding. Nature. 2007;447:316–20. https://doi.org/10.1038/nature05766.

    Article  CAS  PubMed  Google Scholar 

  40. Wang X, Wang X, Liu J, Cai T, Guo L, Wang S, et al. Hair follicle and sebaceous gland de novo regeneration with cultured epidermal stem cells and skin-derived precursors. Stem Cells Transl Med. 2016;5:1695–706. https://doi.org/10.5966/sctm.2015-0397.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Mcheik JN, Barrault C, Levard G, Morel F, Bernard FX, Lecron JC. Epidermal healing in burns: autologous keratinocyte transplantation as a standard procedure: update and perspective. Plast Reconstr Surg Glob Open. 2014;2:e218. https://doi.org/10.1097/GOX.0000000000000176.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Biernaskie J, Paris M, Morozova O, Fagan BM, Marra M, Pevny L, et al. SKPs derive from hair follicle precursors and exhibit properties of adult dermal stem cells. Cell Stem Cell. 2009;5:610–23. https://doi.org/10.1016/j.stem.2009.10.019.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Agabalyan NA, Borys BS, Sparks HD, Boon K, Raharjo EW, Abbasi S, et al. Enhanced expansion and sustained inductive function of skin-derived precursor cells in computer-controlled stirred suspension bioreactors. Stem Cells Transl Med. 2017;6:434–43. https://doi.org/10.5966/sctm.2016-0133.

    Article  CAS  PubMed  Google Scholar 

  44. Cohen J. The transplantation of individual rat and guinea pig whisker papillae. J Embryol Exp Morphol. 1961;9:117–27.

    CAS  PubMed  Google Scholar 

  45. Sabapathy V, Kumar S. hiPSC-derived iMSCs: NextGen MSCs as an advanced therapeutically active cell resource for regenerative medicine. J Cell Mol Med. 2016;20:1571–88. https://doi.org/10.1111/jcmm.12839.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Zhu WY, Zhang RZ, Ma HJ, Wang DG. Isolation and culture of amelanotic melanocytes from human hair follicles. Pigment Cell Res. 2004;17:668–73. https://doi.org/10.1111/j.1600-0749.2004.00190.x.

    Article  PubMed  Google Scholar 

  47. Kumar A, Mohanty S, Sahni K, Kumar R, Gupta S. Extracted hair follicle outer root sheath cell suspension for pigment cell restoration in vitiligo. J Cutan Aesthet Surg. 2013;6:121–5. https://doi.org/10.4103/0974-2077.112679.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Sieber-Blum M, Grim M, Hu YF, Szeder V. Pluripotent neural crest stem cells in the adult hair follicle. Dev Dyn. 2004;231:258–69. https://doi.org/10.1002/dvdy.20129.

    Article  CAS  PubMed  Google Scholar 

  49. Zabierowski SE, Fukunaga-Kalabis M, Li L, Herlyn M. Dermis derived stem cells: a source of epidermal melanocytes and melanoma? Pigment Cell Melanoma Res. 2011;24:422–9. https://doi.org/10.1111/j.1755-148X.2011.00847.x.

    Article  CAS  PubMed  Google Scholar 

  50. Toma JG, Akhavan M, Fernandes KJ, Barnabé-Heider F, Sadikot A, Kaplan DR, et al. Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nat Cell Biol. 2001;3:778–84. https://doi.org/10.1038/ncb0901-778.

    Article  CAS  PubMed  Google Scholar 

  51. Fernandes KJ, McKenzie IA, Mill P, Smith KM, Akhavan M, Barnabé-Heider F, et al. A dermal niche for multipotent adult skin-derived precursor cells. Nat Cell Biol. 2004;6:1082–93. https://doi.org/10.1038/ncb1181.

    Article  CAS  PubMed  Google Scholar 

  52. McKenzie IA, Biernaskie J, Toma JG, Midha R, Miller FD. Skin-derived precursors generate myelinating Schwann cells for the injured and dysmyelinated nervous system. J Neurosci. 2006;26:6651–60. https://doi.org/10.1523/JNEUROSCI.1007-06.2006.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Hunt DP, Morris PN, Sterling J, Anderson JA, Joannides A, Jahoda C, et al. A highly enriched niche of precursor cells with neuronal and glial potential within the hair follicle dermal papilla of adult skin. Stem Cells. 2008;26:163–72.

    Article  CAS  PubMed  Google Scholar 

  54. Krause MP, Dworski S, Feinberg K, Jones K, Johnston AP, Paul S, et al. Direct genesis of functional rodent and human Schwann cells from skin mesenchymal precursors. Stem Cell Rep. 2014;3:85–100. https://doi.org/10.1016/j.stemcr.2014.05.011.

    Article  CAS  Google Scholar 

  55. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, et al. Introduction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell. 2007;131:861–72. https://doi.org/10.1016/j.cell.2007.11.019.

    Article  CAS  PubMed  Google Scholar 

  56. Yang R, Zheng Y, Burrows M, Liu S, Wei Z, Nace A, et al. Generation of folliculogenic human epithelial stem cells from induced pluripotent stem cells. Nat Commun. 2014;5:3071. https://doi.org/10.1038/ncomms4071.

    Article  CAS  PubMed  Google Scholar 

  57. Billingham RE, Medawar P. Technique of free skin grafting in mammals. J Exp Biol. 1950;28:385–402.

    Google Scholar 

  58. Karasek M. In vitro culture of human skin epithelial cell. J Invest Dermatol. 1966;47:533–40.

    Article  CAS  PubMed  Google Scholar 

  59. Moscona A, Moscona H. The dissociation and aggregation of cells from organ rudiments of the early chick embryo. J Anat. 1952;86:287–301.

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Bell E, Ehrlich HP, Buttle DJ, Nakatsuji T. Living tissue formed in vitro and accepted as skin-equivalent tissue of full thickness. Science. 1981;211:1052–4.

    Article  CAS  PubMed  Google Scholar 

  61. Boyce ST, Goretsky MJ, Greenhalgh DG, Kagan RJ, Rieman MT, Warden GD. Comparative assessment of cultured skin substitutes and native skin autograft for treatment of full thickness burns. Ann Surg. 1995;222:743–52.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Delvoye P, Pierard D, Noel A, Nusgens B, Foidart JM, Lapiere CM. Fibroblasts induce the assembly of the macromolecules of the basement membrane. J Invest Dermatol. 1988;90:276–82.

    Article  CAS  PubMed  Google Scholar 

  63. Burke JF, Yannas IV, Quinby WC Jr, Bondoc CC, Jung WK. Successful use of a physiologically acceptable artificial skin in the treatment of extensive burn injury. Ann Surg. 1981;194:413–28.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Zeng W, Zhang S, Liu D, Chai M, Wang J, Zhao Y. Preclinical safety studies on autologous cultured human skin fibroblast transplantation. Cell Transplant. 2014;23:39–49. https://doi.org/10.3727/096368912X659844.

    Article  PubMed  Google Scholar 

  65. Philpott MP, Green MR, Kealey T. Human hair growth in vitro. J Cell Sci. 1990;97:463–71.

    CAS  PubMed  Google Scholar 

  66. Aoki S, Takezawa T, Sugihara H, Toda S. Progress in cell culture systems for pathological research. Pathol Int. 2016;66:554–62. https://doi.org/10.1111/pin.12443.

    Article  PubMed  Google Scholar 

  67. Hayflick L. The limited in vitro lifetime of human diploid cell strains. Exp Cell Res. 1965;37:614–36.

    Article  CAS  PubMed  Google Scholar 

  68. Kiyono T, Foster SA, Koop JI, McDougall JK, Galloway DA, Klingelhutz AJ. Both Rb/p16INK4a inactivation and telomerase activity are required to immortalize human epithelial cells. Nature. 1998;396:84–8. https://doi.org/10.1038/23962.

    Article  CAS  PubMed  Google Scholar 

  69. Hayflick L, Moorhead PS. The serial cultivation of human diploid cell strains. Exp Cell Res. 1961;25:585–621.

    Article  CAS  PubMed  Google Scholar 

  70. Cong YS, Wright WE, Shay JW. Human telomerase and its regulation. Microbiol Mol Biol Rev. 2002;66:407–25.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Blanpain C, Fuchs E. Epidermal homeostasis: a balancing act of stem cells in the skin. Nat Rev Mol Cell Biol. 2009;10:207–17. https://doi.org/10.1038/nrm2636.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Toma JG, McKenzie IA, Bagli D, Miller FD. Isolation and characterization of multipotent skin-derived precursors from human skin. Stem Cells. 2005;23:727–37. https://doi.org/10.1634/stemcells.2004-0134.

    Article  CAS  PubMed  Google Scholar 

  73. Malik N, Rao MS. A review of the methods for human iPSC derivation. Methods Mol Biol. 2013;997:23–33. https://doi.org/10.1007/978-1-62703-348-0_3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Eça LP, Pinto DG, de Pinho AM, Mazzetti MP, Odo ME. Autologous fibroblast culture in the repair of aging skin. Dermatol Surg. 2012;38:180–4. https://doi.org/10.1111/j.1524-4725.2011.02192.x.

    Article  CAS  PubMed  Google Scholar 

  75. Phillips CL, Combs SB, Pinnell SR. Effects of ascorbic acid on proliferation and collagen synthesis in relation to the donor age of human dermal fibroblasts. J Invest Dermatol. 1994;103:228–32.

    Article  CAS  PubMed  Google Scholar 

  76. Woan KV, Narain NR, Persaud I, et al. Coenzyme Q10 enhances the proliferation and migration of fibroblasts and keratinocytes: a possible implication for wound healing. J Invest Dermatol. 2005;124s:A57.

    Google Scholar 

  77. Dame MK, Spahlinger DM, DaSilva M, Perone P, Dunstan R, Varani J. Establishment and characteristics of Gottingen minipig skin in organ culture and monolayer cell culture: relevance to drug safety testing. In Vitro Cell Dev Biol Anim. 2008;44(7):245–52. https://doi.org/10.1007/s11626-008-9091-3.

    Article  PubMed  Google Scholar 

  78. Solakoglu S, Tiryaki T, Ciloglu SE. The effect of cultured autologous fibroblasts on longevity of cross-linked hyaluronic acid used as a filler. Aesthet Surg J. 2008;28:412–6. https://doi.org/10.1016/j.asj.2008.04.008.

    Article  PubMed  Google Scholar 

  79. Weiss RA. Autologous cell therapy: will it replace dermal fillers? Facial Plast Surg Clin North Am. 2013;21:299–304. https://doi.org/10.1016/j.fsc.2013.02.008.

    Article  PubMed  Google Scholar 

  80. Zhao Y, Wang J, Yan X, Li D, Xu J. Preliminary survival studies on autologous cultured skin fibroblasts transplantation by injection. Cell Transplant. 2008;17:775–83.

    Article  PubMed  Google Scholar 

  81. Eves PC, Beck AJ, Shard AG, Mac NS. A chemically defined surface for the co-culture of melanocytes and keratinocytes. Biomaterials. 2005;26:7068–81. https://doi.org/10.1016/j.biomaterials.2005.05.015.

    Article  CAS  PubMed  Google Scholar 

  82. Matsumoto T, Kano K, Kondo D, Fukuda N, Iribe Y, Tanaka N, et al. Mature adipocyte-derived dedifferentiated fat cells exhibit multilineage potential. J Cell Physiol. 2008;215:210–22. https://doi.org/10.1002/jcp.21304.

    Article  CAS  PubMed  Google Scholar 

  83. Bayati V, Gazor R, Nejatbakhsh R, Negad DF. Enrichment of skin-derived neural precursor cells from dermal cell populations by altering culture conditions. Stem Cell Invest. 2016;3:83–92. https://doi.org/10.21037/sci.2016.10.10.

    Article  CAS  Google Scholar 

  84. Bickenbach JR. Isolation, characterization, and culture of epithelial stem cells. Methods Mol Biol. 2005;289:97–102.

    PubMed  Google Scholar 

  85. Lee MJ, Kim J, Lee KI, Shin JM, Chae JI, Chung HM. Enhancement of wound healing by secretory factors of endothelial precursor cells derived from human embryonic stem cells. Cytotherapy. 2011;13:165–78. https://doi.org/10.3109/14653249.2010.512632.

    Article  CAS  PubMed  Google Scholar 

  86. Levenberg S, Golub JS, Amit M, Itskovitz-Eldor J, Langer R. Endothelial cells derived from human embryonic stem cells. Proc Natl Acad Sci U S A. 2002;99:4391–6. https://doi.org/10.1073/pnas.032074999.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Monaco JL, Lawrence WT. Acute wound healing an overview. Clin Plast Surg. 2003;30:1–12.

    Article  PubMed  Google Scholar 

  88. Westgate GE, Gibson WT, Kealey T, Philpott MP. Prolonged maintenance of human hair follicles in vitro in a serum-free medium. Br J Dermatol. 1993;129:372–9.

    Article  CAS  PubMed  Google Scholar 

  89. Purba TS, Haslam IS, Poblet E, Jiménez F, Gandarillas A, Izeta A, et al. Human epithelial hair follicle stem cells and their progeny: current state of knowledge, the widening gap in translational research and future challenges. BioEssays. 2014;36:513–25. https://doi.org/10.1002/bies.201300166.

    Article  CAS  PubMed  Google Scholar 

  90. Brown TD. Techniques for mechanical stimulation of cells in vitro: a review. J Biomech. 2000;33:3–14.

    Article  CAS  PubMed  Google Scholar 

  91. Huang HL, Hsing HW, Lai TC, Chen YW, Lee TR, Chan HT. Trypsin-induced proteome alteration during cell subculture in mammalian cells. J Biomed Sci. 2010;17:36. https://doi.org/10.1186/1423-0127-17-36.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Yamada N, Okano T, Sakai H, Karikusa F, Sawasaki Y, Sakurai Y. Thermoresponsive polymeric surfaces: control of attachment and detachment of cultured cells. Makromol Chem Rapid Commun. 1990;11:571–6. https://doi.org/10.1002/marc.1990.030111109.

    Article  CAS  Google Scholar 

  93. Yang L, Cheng F, Liu T, Lu JR, Song K, Jiang L, et al. Comparison of mesenchymal stem cells released from poly(N-isopropylacrylamide) copolymer film and by trypsinization. Biomed Mater. 2012;7:035003. https://doi.org/10.1088/1748-6041/7/3/035003.

    Article  CAS  PubMed  Google Scholar 

  94. Ozbun MA, Patterson NA. Using organotypic (raft) epithelial tissue cultures for the biosynthesis and isolation of infectious human papillomaviruses. Curr Protoc Microbiol. 2014;34:14B.3.1–18. https://doi.org/10.1002/9780471729259.mc14b03s34.

    Article  Google Scholar 

  95. Brindley D, Moorthy K, Lee JH, Mason C, Kim HW, Wall I. Bioprocess forces and their impact on cell behavior: implications for bone regeneration therapy. J Tissue Eng. 2011;2011:620247. https://doi.org/10.4061/2011/620247.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Gareau T, Lara GG, Shepherd RD, Krawetz R, Rancourt DE, Rinker KD, et al. Shear stress influences the pluripotency of murine embryonic stem cells in stirred suspension bioreactors. J Tissue Eng Regen Med. 2014;8:268–78. https://doi.org/10.1002/term.1518.

    Article  CAS  PubMed  Google Scholar 

  97. Hakim N, editor. Artificial organs, new techniques in surgery series 4. Springer-Verlag London Limited; 2009. https://doi.org/10.1007/978-1-84882-283-2_6.

    Chapter  Google Scholar 

  98. Cubo N, Garcia M, Del Cañizo JF, Velasco D, Jorcano JL. 3D bioprinting of functional human skin: production and in vivo analysis. Biofabrication. 2016;9:015006. https://doi.org/10.1088/1758-5090/9/1/015006.

    Article  CAS  PubMed  Google Scholar 

  99. Pandey AR, Singh US, Momin M, et al. J Polym Res. 2017;24:125. https://doi.org/10.1007/s10965-017-1286-4.

    Article  CAS  Google Scholar 

  100. MacNeil S. Progress and opportunities for tissue-engineered skin. Nature. 2007;445:874–80. https://doi.org/10.1038/nature05664.

    Article  CAS  PubMed  Google Scholar 

  101. Kubo K, Kuroyanagi Y. A study of cytokines released from fibroblasts in cultured dermal substitute. Artif Organs. 2005;29:845–9. https://doi.org/10.1111/j.1525-1594.2005.00138.x.

    Article  CAS  PubMed  Google Scholar 

  102. Moustafa M, Simpson C, Glover M, Dawson RA, Tesfaye S, Creagh FM, et al. A new autologous keratinocyte dressing treatment for non-healing diabetic neuropathic foot ulcers. Diabet Med. 2004;21:786–9.

    Article  CAS  PubMed  Google Scholar 

  103. Zhu N, Warner RM, Simpson C, Glover M, Hernon CA, Kelly J, et al. Treatment of burns and chronic wounds using a new cell transfer dressing for delivery of autologous keratinocytes. Eur J Plast Surg. 2005;28:319–30.

    Article  Google Scholar 

  104. 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.

    Article  CAS  PubMed  Google Scholar 

  105. Carsin H, Ainaud P, Le Bever H, Rives J, Lakhel A, Stephanazzi J, et al. Cultured epithelial autografts in extensive burn coverage of severely traumatized patients: a five year single-center experience with 30 patients. Burns. 2000;26:379–87.

    Article  CAS  PubMed  Google Scholar 

  106. Tausche AK, Skaria M, Böhlen 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.

    Article  PubMed  Google Scholar 

  107. Renner R, Harth W, Simon JC. Transplantation of chronic wounds with epidermal sheets derived from autologous hair follicle--the Leipzig experience. Int Wound J. 2009;6:226–32. https://doi.org/10.1111/j.1742-481X.2009.00609.x.

    Article  PubMed  PubMed Central  Google Scholar 

  108. Wainwright DJ. Use of an acellular allograft dermal matrix (AlloDerm) in the management of full-thickness burns. Burns. 1995;21:243–8.

    Article  CAS  PubMed  Google Scholar 

  109. Gordley K, Cole P, Hicks J, Hollier L. A comparative, long term assessment of soft tissue substitutes: AlloDerm, Enduragen, and Dermamatrix. J Plast Reconstr Aesthet Surg. 2009;62:849–50. https://doi.org/10.1016/j.bjps.2008.05.006.

    Article  PubMed  Google Scholar 

  110. Cooper ML, Hansbrough JF, Spielvogel RL, Cohen R, Bartel RL, Naughton G. In vivo optimization of a living dermal substitute employing cultured human fibroblasts on a biodegradable polyglycolic acid or polyglactin mesh. Biomaterials. 1991;12:243–8.

    Article  CAS  PubMed  Google Scholar 

  111. Kearney JN. Clinical evaluation of skin substitutes. Burns. 2001;27:545–51.

    Article  CAS  PubMed  Google Scholar 

  112. Branski LK, Herndon DN, Pereira C, Mlcak RP, Celis MM, Lee JO, et al. Longitudinal assessment of Integra in primary burn management: a randomized pediatric clinical trial. Crit Care Med. 2007;35:2615–23. https://doi.org/10.1097/01.CCM.0000285991.36698.E2.

    Article  PubMed  Google Scholar 

  113. Stiefel D, Schiestl C, Meuli M. Integra artificial skin for burn scar revision in adolescents and children. Burns. 2010;36:114–20. https://doi.org/10.1016/j.burns.2009.02.023.

    Article  PubMed  Google Scholar 

  114. Haslik W, Kamolz LP, Nathschläger G, Andel H, Meissl G, Frey M. First experiences with the collagen-elastin matrix Matriderm as a dermal substitute in severe burn injuries of the hand. Burns. 2007;33:364–8. https://doi.org/10.1016/j.burns.2006.07.021.

    Article  CAS  PubMed  Google Scholar 

  115. Schneider J, Biedermann T, Widmer D, Montano I, Meuli M, Reichmann E, et al. Matriderm versus Integra: a comparative experimental study. Burns. 2009;35:51–7. https://doi.org/10.1016/j.burns.2008.07.018.

    Article  PubMed  Google Scholar 

  116. 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. https://doi.org/10.1098/rsif.2009.0403.

    Article  CAS  PubMed  Google Scholar 

  117. Sheridan RL, Morgan JR, Cusick JL, Petras LM, Lydon MM, Tompkins RG. Initial experience with a composite autologous skin substitute. Burns. 2001;27:421–4.

    Article  CAS  PubMed  Google Scholar 

  118. Keck M, Haluza D, Lumenta DB, Burjak S, Eisenbock B, Kamolz LP, et al. Construction of a multi-layer skin substitute: simultaneous cultivation of keratinocytes and preadipocytes on a dermal template. Burns. 2011;37:626–30. https://doi.org/10.1016/j.burns.2010.07.016.

    Article  PubMed  Google Scholar 

  119. Gómez C, Galán JM, Torrero V, Ferreiro I, Pérez D, Palao R, et al. Use of an autologous bioengineered composite skin in extensive burns: clinical and functional outcomes. A multicentric study. Burns. 2011;37:580–9. https://doi.org/10.1016/j.burns.2010.10.005.

    Article  PubMed  Google Scholar 

  120. Kirsner RS. The use of Apligraf in acute wounds. J Dermatol. 1998;25:805–11.

    CAS  PubMed  Google Scholar 

  121. Edmonds M, European and Australian Apligraf Diabetic Foot Ulcer Study Group. Apligraf in the treatment of neuropathic diabetic foot ulcers. Int J Low Extrem Wounds. 2009;8:11–8. https://doi.org/10.1177/1534734609331597.

    Article  PubMed  Google Scholar 

  122. Eisenberg M, Llewellyn DM, Moran K, Kerr A. Successful engraftment of cultured human epidermal allograft in a child with recessive dystrophic epidermolysis bullosa. Med J Aust. 1987;147:520–1.

    CAS  PubMed  Google Scholar 

  123. Windsor ML, Eisenberg M, Gordon-Thomson C, Moore GP. A novel model of wound healing in the SCID mouse using a cultured human skin substitute. Australas J Dermatol. 2009;50:29–35. https://doi.org/10.1111/j.1440-0960.2008.00512.x.

    Article  PubMed  Google Scholar 

  124. Tavis MJ, Thornton JW, Bartlett RH, et al. A new composite skin prosthesis. Burns. 1979;8:123–30.

    Google Scholar 

  125. Demling RH, DeSanti L. Management of partial thickness facial burns (comparison of topical antibiotics and bio-engineered skin substitutes). Burns. 1999;25:256–61.

    Article  CAS  PubMed  Google Scholar 

  126. Wood FM, Kolybaba ML, Allen P. The use of cultured epithelial autograft in the treatment of major burn injuries: a critical review of the literature. Burns. 2006;32:395–401. https://doi.org/10.1016/j.burns.2006.01.008.

    Article  CAS  PubMed  Google Scholar 

  127. Meuli M, Raghunath M. Burns (Part 2). Tops and flops using cultured epithelial autografts in children. Pediatr Surg Int. 1997;12:471–7.

    CAS  PubMed  Google Scholar 

  128. Horch RE, Kopp J, Kneser U, Beier J, Bach AD. Tissue engineering of cultured skin substitutes. J Cell Mol Med. 2005;9:592–608.

    Article  PubMed  PubMed Central  Google Scholar 

  129. Wood FM. Clinical potential of cellular autologous epithelial suspension. Wounds. 2002;15:16–22.

    Google Scholar 

  130. Pham C, Greenwood J, Cleland H, Woodruff P, Maddern G. Bioengineered skin substitutes for the management of burns: a systematic review. Burns. 2007;33:946–57. https://doi.org/10.1016/j.burns.2007.03.020.

    Article  PubMed  Google Scholar 

  131. Mansbridge J. Commercial considerations in tissue engineering. J Anat. 2006;209:527–32. https://doi.org/10.1111/j.1469-7580.2006.00631.x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Wood FM, Stoner ML, Fowler BV, Fear MW. The use of a non-cultured autologous cell suspension and Integra dermal regeneration template to repair full-thickness skin wounds in a porcine model: a one-step process. Burns. 2007;33:693–700. https://doi.org/10.1016/j.burns.2006.10.388.

    Article  PubMed  Google Scholar 

  133. Boyce ST. Design principles for composition and performance of cultured skin substitutes. Burns. 2001;27:523–33.

    Article  CAS  PubMed  Google Scholar 

  134. Sabeh G, Sabé M, Ishak S, Sweid R, Ayoubi M, Chahal AM. Greffes séquentielles de cellules cutanées: premiers résultats d’un nouveau procédé et revue de la littérature. J Med Liban. 2015;63:47–58.

    PubMed  Google Scholar 

  135. Driskell RR, Clavel C, Rendl M, Watt FM. Hair follicle dermal papilla cells at a glance. J Cell Sci. 2011;124:1179–82. https://doi.org/10.1242/jcs.082446.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Hu MS, Rennert RC, McArdle A, Chung MT, Walmsley GG, Longaker MT, Lorenz HP. The role of stem cells during scarless skin wound healing. Adv Wound Care (New Rochelle). 2014;3:304–14. https://doi.org/10.1089/wound.2013.0471.

    Article  PubMed Central  Google Scholar 

  137. Chun-mao H, Su-yi W, Ping-ping L, Hang-hui C. Human bone marrow-derived mesenchymal stem cells differentiate into epidermal-like cells in vitro. Differentiation. 2007;75:292–8. https://doi.org/10.1111/j.1432-0436.2006.00140.x.

    Article  CAS  PubMed  Google Scholar 

  138. Wang C, Lin K, Chang J, Sun J. Osteogenesis and angiogenesis induced by porous beta-CaSiO(3)/PDLGA composite scaffold via activation of AMPK/ERK1/2 and PI3K/Akt pathways. Biomaterials. 2013;34(1):64–77. https://doi.org/10.1016/j.biomaterials.2012.09.021.

    Article  CAS  PubMed  Google Scholar 

  139. Kim HJ, Park SS, Oh SY, Kim H, Kweon OK, Woo HM, et al. Effect of acellular dermal matrix as a delivery carrier of adipose-derived mesenchymal stem cells on bone regeneration. J Biomed Mater Res B Appl Biomater. 2012;100:1645–53. https://doi.org/10.1002/jbm.b.32733.

    Article  CAS  PubMed  Google Scholar 

  140. Burd A, Chiu T. Allogeneic skin in the treatment of burns. Clin Dermatol. 2005;23:376–87. https://doi.org/10.1016/j.clindermatol.2004.07.019.

    Article  PubMed  Google Scholar 

  141. Waymack P, Duff RG, Sabolinski M. The effect of a tissue engineered bilayered living skin analog, over meshed split-thickness autografts on the healing of excised burn wounds. The Apligraf Burn Study Group. Burns. 2000;26:609–19.

    Article  CAS  PubMed  Google Scholar 

  142. Gath HJ, Hell B, Zarrinbal R, Bier J, Raguse JD. Regeneration of intraoral defects after tumour resection with a bioengineered human dermal replacement (Dermagraft). Plast Reconstr Surg. 2002;109:889–93.

    Article  PubMed  Google Scholar 

  143. Gohari S, Gambla C, Healey M, Spaulding G, Gordon KB, Swan J, et al. Evaluation of tissue-engineered skin (human skin substitute) and secondary intention healing in the treatment of full thickness wounds after Mohs micrographic or excisional surgery. Dermatol Surg. 2002;28:1107–14.

    PubMed  Google Scholar 

  144. Moon KC, Lee HS, Han SK, et al. Aesth Plast Surg. 2018;42:815. https://doi.org/10.1007/s00266-017-1044-3.

    Article  Google Scholar 

  145. Watson D, Keller GS, Lacombe V, Fodor PB, Rawnsley J, Lask GP. Autologous fibroblasts for treatment of facial rhytids and dermal depressions: a pilot study. Arch Facial Plast Surg. 1999;1:165–70.

    Article  CAS  PubMed  Google Scholar 

  146. Gonzalez MJ, Sturgill WH, Ross EV, Uebelhoer NS. Treatment of acne scars using the plasma skin regeneration (PSR) system. Lasers Surg Med. 2008;40:124–7. https://doi.org/10.1002/lsm.20617.

    Article  PubMed  Google Scholar 

  147. Velander P, Theopold C, Bleiziffer O, Bergmann J, Svensson H, Feng Y, et al. Cell suspensions of autologous keratinocytes or autologous fibroblasts accelerate the healing of full thickness skin wounds in a diabetic porcine wound healing model. J Surg Res. 2009;157:14–20. https://doi.org/10.1016/j.jss.2008.10.001.

    Article  CAS  PubMed  Google Scholar 

  148. Li J, Chen J, Kirsner R. Pathophysiology of acute wound healing. Clin Dermatol. 2007;25:9–18. https://doi.org/10.1016/j.clindermatol.2006.09.007.

    Article  CAS  PubMed  Google Scholar 

  149. Weiss RA, Weiss MA, Beasley KL, Munavalli G. Autologous cultured fibroblast injection for facial contour deformities: a prospective, placebo-controlled, phase III clinical trial. Dermatol Surg. 2007;33:263–8. https://doi.org/10.1111/j.1524-4725.2007.33060.x.

    Article  CAS  PubMed  Google Scholar 

  150. Smith SR, Munavalli G, Weiss R, Maslowski JM, Hennegan KP, Novak JM. A multicenter, double-blind, placebo-controlled trial of autologous fibroblast therapy for the treatment of nasolabial fold wrinkles. Dermatol Surg. 2012;38:1234–43. https://doi.org/10.1111/j.1524-4725.2012.02349.x.

    Article  CAS  PubMed  Google Scholar 

  151. Narins RS, Brandt FS, Lorenc ZP, Maas CS, Monheit GD, Smith SR. Twelve-month persistency of a novel ribose-cross-linked collagen dermal filler. Dermatol Surg. 2008;3:S31–9. https://doi.org/10.1111/j.1524-4725.2008.34240.x.

    Article  CAS  Google Scholar 

  152. Smith SR, Jones D, Thomas JA, Murphy DK, Beddingfield FC 3rd. Duration of wrinkle correction following repeat treatment with Juvederm hyaluronic acid fillers. Arch Dermatol Res. 2010;302:757–62. https://doi.org/10.1007/s00403-010-1086-8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. Yoon ES, Han SK, Kim WK. Advantages of the presence of living dermal fibroblasts within restylane for soft tissue augmentation. Ann Plast Surg. 2003;51:587–92. https://doi.org/10.1097/01.sap.0000096424.23397.2a.

    Article  PubMed  Google Scholar 

  154. Muir I, Padilla-Lamb A, Stewart JE, Wheatley DN. Growth inhibition of culture fibroblast by extracts from human dermis. Br J Plast Surg. 1997;50:186–93.

    Article  CAS  PubMed  Google Scholar 

  155. Lee HJ, Lee EG, Kang S, Sung JH, Chung HM, Kim DH. Efficacy of microneedling plus human stem cell conditioned medium for skin rejuvenation: a randomized, controlled, blinded split-face study. Ann Dermatol. 2014;26:584–91. https://doi.org/10.5021/ad.2014.26.5.584.

    Article  PubMed  PubMed Central  Google Scholar 

  156. Wu Y, Wang J, Scott PG, Tredget EE. Bone marrow-derived stem cells in wound healing: a review. Wound Repair Regen. 2007;15:S18–26. https://doi.org/10.1111/j.1524-475X.2007.00221.x.

    Article  PubMed  Google Scholar 

  157. Thomas ED, Lochte HL Jr, Cannon JH, Sahler OD, Ferrebee JW. Supralethal whole body irradiation and isologous marrow transplantation in man. J Clin Invest. 1959;38:1709–16. https://doi.org/10.1172/JCI103949.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Gragnani A, Giannoccaro FB, Sobral CS, Moraes AA, França JP, Ferreira AT, et al. Dimethylaminoethanol affects the viability of human cultured fibroblasts. Aesthet Plast Surg. 2007;31:711–8. https://doi.org/10.1007/s00266-006-0208-3.

    Article  Google Scholar 

  159. Falanga V, Margolis D, Alvarez O, Auletta M, Maggiacomo F, Altman M, et al. Rapid healing of venous ulcers and lack of clinical rejection with an allogeneic cultured human skin equivalent. Human skin equivalent investigators group. Arch Dermatol. 1998;134:293–300.

    Article  CAS  PubMed  Google Scholar 

  160. Theobald VA, Lauer JD, Kaplan FA, Baker KB, Rosenberg M. ‘Neutral allografts’—lack of allogeneic stimulation by cultured human cells expressing MHC class I and class II antigens. Transplantation. 1993;55:128–33.

    Article  CAS  PubMed  Google Scholar 

  161. Phillips TJ, Manzoor J, Rojas A, Isaacs C, Carson P, Sabolinski M, et al. The longevity of a bilayered skin substitute after application to venous ulcers. Arch Dermatol. 2002;138:1079–81.

    PubMed  Google Scholar 

  162. Price RD, Das-Gupta V, Harris PA, Leigh IM, Navsaria HA. The role of allogenic fibroblasts in an acute wound healing model. Plast Reconstr Surg. 2004;113:1719–29.

    Article  PubMed  Google Scholar 

  163. Barnas JL, Simpson-Abelson MR, Brooks SP, Kelleher RJ Jr, Bankert RB. Reciprocal functional modulation of the activation of T lymphocytes and fibroblasts derived from human solid tumors. J Immunol. 2010;185(5):2681–92. https://doi.org/10.4049/jimmunol.1000896.

    Article  CAS  PubMed  Google Scholar 

  164. Mazlyzam AL, Aminuddin BS, Saim L, Ruszymah BH. Human serum is an advantageous supplement for human dermal fibroblast expansion: clinical implications for tissue engineering of skin. Arch Med Res. 2008;39:743–52. https://doi.org/10.1016/j.arcmed.2008.09.001.

    Article  CAS  PubMed  Google Scholar 

  165. Griffiths M, Ojeh N, Livingstone R, Price R, Navsaria H. Survival of Apligraf in acute human wounds. Tissue Eng. 2004;10:1180–95. https://doi.org/10.1089/ten.2004.10.1180.

    Article  CAS  PubMed  Google Scholar 

  166. 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. https://doi.org/10.1016/S0140-6736(09)61496-3.

    Article  CAS  PubMed  Google Scholar 

  167. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, et al. Embryonic stem cells lines derived from human blastocysts. Science. 1998;282:1145–7.

    Article  CAS  PubMed  Google Scholar 

  168. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006;126:663–76. https://doi.org/10.1016/j.cell.2006.07.024.

    Article  CAS  PubMed  Google Scholar 

  169. Ng WL, Wang S, Yeong WY, Naing MW. Skin bioprinting: impending reality or fantasy? Trends Biotechnol. 2017;35:278. https://doi.org/10.1016/j.tibtech.2016.08.009.

    Article  CAS  PubMed  Google Scholar 

  170. Augustine R. Prog Biomater. 2018;7:77. https://doi.org/10.1007/s40204-018-0087-0.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  171. Koch L, Deiwick A, Schlie S, Michael S, Gruene M, Coger V, et al. Skin tissue generation by laser cell printing. Biotechnol Bioeng. 2012;109:1855–63. https://doi.org/10.1002/bit.24455. Epub 2012 Feb 13.

    Article  CAS  PubMed  Google Scholar 

  172. Michael S, Sorg H, Peck CT, Koch L, Deiwick A, Chichkov B, et al. Tissue engineered skin substitutes created by laser-assisted bioprinting form skin-like structures in the dorsal skin fold chamber in mice. PLoS One. 2013;8:e57741. https://doi.org/10.1371/journal.pone.0057741.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  173. Lee V, Singh G, Trasatti JP, Bjornsson C, Xu X, Tran TN, et al. Design and fabrication of human skin by three-dimensional bioprinting. Tissue Eng Part C Methods. 2014;20:473–84. https://doi.org/10.1089/ten.TEC.2013.0335.

    Article  CAS  PubMed  Google Scholar 

  174. Lee W, Lee V, Polio S, Keegan P, Lee JH, Fischer K, et al. On-demand three-dimensional freeform fabrication of multi-layered hydrogel scaffold with fluidic channels. Biotechnol Bioeng. 2010;105:1178–86. https://doi.org/10.1002/bit.22613.

    Article  CAS  PubMed  Google Scholar 

  175. Lee W, Debasitis JC, Lee VK, Lee JH, Fischer K, Edminster K, et al. Multi-layered culture of human skin fibroblasts and keratinocytes through three-dimensional freeform fabrication. Biomaterials. 2009;30:1587–95. https://doi.org/10.1016/j.biomaterials.2008.12.009.

    Article  CAS  PubMed  Google Scholar 

  176. Hussein SM, Nagy K, Nagy A. Human induced pluripotent stem cells: the past, present, and future. Clin Pharmacol Ther. 2011;89:741–5. https://doi.org/10.1038/clpt.2011.37.

    Article  CAS  PubMed  Google Scholar 

  177. Yamanaka S. Induced pluripotent stem cells: past, present, and future. Cell Stem Cell. 2012;10:678–84. https://doi.org/10.1016/j.stem.2012.05.005.

    Article  CAS  PubMed  Google Scholar 

  178. Turksen K. Revisiting the bulge. Dev Cell. 2004;6:454–6.

    Article  CAS  PubMed  Google Scholar 

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Jáñez, L. (2019). Skin Cell Cultures and Skin Engineering. In: Pinto, H., Fontdevila, J. (eds) Regenerative Medicine Procedures for Aesthetic Physicians. Springer, Cham. https://doi.org/10.1007/978-3-030-15458-5_15

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