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Tissue engineering of oral mucosa: a shared concept with skin

  • Review
  • Tissue Engineering / Regenerative Medicine
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Abstract

Tissue-engineered oral mucosa, in the form of epithelial cell sheets or full-thickness oral mucosa equivalents, is a potential solution for many patients with congenital defects or with tissue loss due to diseases or tumor excision following a craniofacial cancer diagnosis. In the laboratory, it further serves as an in vitro model, alternative to in vivo testing of oral care products, and provides insight into the behavior of the oral mucosal cells in healthy and pathological tissues. This review covers the old and new generation scaffold types and materials used in oral mucosa engineering; discusses similarities and differences between oral mucosa and skin, the methods developed to reconstruct oral mucosal defects; and ends with future perspectives on oral mucosa engineering.

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References

  1. Feinberg SE, Aghaloo TL, Cunningham LL Jr. Role of tissue engineering in oral and maxillofacial reconstruction: findings of the 2005 AAOMS Research Summit. J Oral Maxillofac Surg. 2005;63:1418–25.

    PubMed  Google Scholar 

  2. MacNeil S. Progress and opportunities for tissue-engineered skin. Nature. 2007;445:874–80.

    CAS  PubMed  Google Scholar 

  3. Ueda M, Tohnai I, Nakai H. Tissue engineering research in oral implant surgery. Artif Organs. 2001;25:164–71.

    CAS  PubMed  Google Scholar 

  4. Lauer G. Fundamentals of tissue engineering and regenerative medicine. Berlin Heidelberg: Springer; 2009.

    Google Scholar 

  5. Will J, Melcher R, Treul C, Travitzky N, Kneser U, Polykandriotis E, et al. Porous ceramic bone scaffolds for vascularized bone tissue regeneration. J Mater Sci Mater Med. 2008;19:2781–90.

    CAS  PubMed  Google Scholar 

  6. Squier CA, Kremer MJ. Biology of oral mucosa and esophagus. J Natl Cancer Inst Monogr. 2001;29:7–15.

    PubMed  Google Scholar 

  7. Winning TA, Townsend GC. Oral mucosal embryology and histology. Clin Dermatol. 2000;18:499–511.

    CAS  PubMed  Google Scholar 

  8. 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;32:188–97.

    CAS  PubMed  Google Scholar 

  9. Squier CA. The permeability of oral mucosa. Crit Rev Oral Biol Med. 1991;2:13–32.

    CAS  PubMed  Google Scholar 

  10. Raghoebar GM, Tomson AM, Scholma J, Blaauw EH, Witjes MJ, Vissink A. Use of cultured mucosal grafts to cover defects caused by vestibuloplasty: an in vivo study. J Oral Maxillofac Surg. 1995;53:872–8.

    CAS  PubMed  Google Scholar 

  11. Okano T, Yamada N, Sakai H, Sakurai Y. A novel recovery system for cultured cells using plasma-treated polystyrene dishes grafted with poly(N-isopropylacrylamide). J Biomed Mater Res. 1993;27:1243–51.

    CAS  PubMed  Google Scholar 

  12. Nakamura T, Endo K, Cooper LJ, Fullwood NJ, Tanifuji N, Tsuzuki M, et al. The successful culture and autologous transplantation of rabbit oral mucosal epithelial cells on amniotic membrane. Invest Ophthalmol Vis Sci. 2003;44:106–16.

    PubMed  Google Scholar 

  13. Imaizumi F, Asahina I, Moriyama T, Ishii M, Omura K. Cultured mucosal cell sheet with a double layer of keratinocytes and fibroblasts on a collagen membrane. Tissue Eng. 2004;10:657–64.

    CAS  PubMed  Google Scholar 

  14. Yamada N, Okano T, Sakai H, Karikusa F, Sawasaki Y, Sakurai Y. Thermo-responsive polymeric surfaces; control of attachment and detachment of cultured cells. Makromol Chem Rapid Commun. 1990;11:571–6.

    CAS  Google Scholar 

  15. Yang YJ, Yamato M, Kohno C, Nishimoto A, Sekine H, Fukai F, et al. Cell sheet engineering: recreating tissues without biodegradable scaffolds. Biomaterials. 2005;26:6415–22.

    CAS  PubMed  Google Scholar 

  16. Murakami D, Yamato M, Nishida K, Ohki T, Takagi R, Yang J, et al. Fabrication of transplantable human oral mucosal epithelial cell sheets using temperature-responsive culture inserts without feeder layer cells. J Artif Organs. 2006;9:185–9.

    PubMed  Google Scholar 

  17. Ueda M. Formation of epithelial sheets by serially cultivated human mucosal cells and their applications as a graft material. Nagoya J Med Sci. 1995;58:13–28.

    CAS  PubMed  Google Scholar 

  18. Langdon J, Williams DM, Navsaria H, Leigh IM. Autologous keratinocyte grafting: a new technique for intra-oral reconstruction. Br Dent J. 1991;171:87–90.

    CAS  PubMed  Google Scholar 

  19. Bodner L, Grossman N. Autologous cultured mucosal graft to cover large intraoral mucosal defects: a clinical study. J Oral Maxillofac Surg. 2003;61:169–73.

    PubMed  Google Scholar 

  20. Nishida K, Yamato M, Hayashida Y, Watanabe K, Yamamoto K, Adachi E, et al. Corneal reconstruction with tissue-engineered cell sheets composed of autologous oral mucosal epithelium. N Engl J Med. 2004;351:1187–96.

    CAS  PubMed  Google Scholar 

  21. Inatomi T, Nakamura T, Koizumi N, Sotozono C, Kinoshita S. Current progress and challenges in ocular surface reconstruction using cultivated epithelial sheet transplantation. Med J Malaysia 2008;63:Suppl A:42.

  22. Satake Y, Higa K, Tsubota K, Shimazaki J. Long-term outcome of cultivated oral mucosal epithelial sheet transplantation in treatment of total limbal stem cell deficiency. Ophthalmology. 2011;118:1524–30.

    PubMed  Google Scholar 

  23. Burillon C, Huot L, Justin V, Nataf S, Chapuis F, Decullier E, et al. Cultured autologous oral mucosal epithelial cell sheet (CAOMECS) transplantation for the treatment of corneal limbal stem cell deficiency. Invest Ophthalmol Vis Sci. 2012;53:1325–31.

    PubMed  Google Scholar 

  24. Sotozono C, Inatomi T, Nakamura T, Koizumi N, Yokoi N, Ueta M, et al. Visual improvement after cultivated oral mucosal epithelial transplantation. Ophthalmology. 2013;120:193–200.

    PubMed  Google Scholar 

  25. Ohki T, Yamato M, Murakami D, Takagi R, Yang J, Namiki H, et al. Treatment of oesophageal ulcerations using endoscopic transplantation of tissue-engineered autologous oral mucosal epithelial cell sheets in a canine model. Gut. 2006;55:1704–10.

    PubMed Central  CAS  PubMed  Google Scholar 

  26. Takagi R, Murakami D, Kondo M, Ohki T, Sasaki R, Mizutani M, et al. Fabrication of human oral mucosal epithelial cell sheets for treatment of esophageal ulceration by endoscopic submucosal dissection. Gastrointest Endosc. 2010;72:1253–9.

    PubMed  Google Scholar 

  27. Watanabe E, Yamato M, Shiroyanagi Y, Tanabe K, Okano T. Bladder augmentation using tissue-engineered autologous oral mucosal epithelial cell sheets grafted on demucosalized gastric flaps. Transplantation. 2011;91:700–6.

    PubMed  Google Scholar 

  28. Gallico GG, O’Conner NE. Engineering a skin replacement. Tissue Eng. 1995;1:231–40.

    CAS  PubMed  Google Scholar 

  29. Dongari-Bagtzoglou A, Kashleva H. Development of a highly reproducible three-dimensional organotypic model of the oral mucosa. Nat Protoc. 2006;1:2012–8.

    PubMed Central  CAS  PubMed  Google Scholar 

  30. Yoshizawa M, Feinberg SE, Marcelo CL, Elner VM. Ex vivo produced human conjunctiva and oral mucosa equivalents grown in a serum-free culture system. J Oral Maxillofac Surg. 2004;62:980–8.

    PubMed  Google Scholar 

  31. Nakanishi Y, Izumi K, Yoshizawa M, Saito C, Kawano Y, Maeda T. The expression and production of vascular endothelial growth factor in oral mucosa equivalents. Int J Oral Maxillofac Surg. 2007;36:928–33.

    CAS  PubMed  Google Scholar 

  32. Xiong X, Zhao Y, Zhang W, Xie W, He S. In vitro engineering of a palatal mucosa equivalent with acellular porcine dermal matrix. J Biomed Mater Res A. 2008;86:544–51.

    PubMed  Google Scholar 

  33. Tra WM, van Neck JW, Hovius SE, van Osch GJ, Perez-Amodio S. Characterization of a three-dimensional mucosal equivalent: similarities and differences with native oral mucosa. Cells Tissues Organs. 2012;195:185–96.

    CAS  PubMed  Google Scholar 

  34. Alaminos M, Garzón I, Sánchez-Quevedo MC, Moreu G, González-Andrades M, Fernández-Montoya A, et al. Time-course study of histological and genetic patterns of differentiation in human engineered oral mucosa. J Tissue Eng Regen Med. 2007;1:350–9.

    CAS  PubMed  Google Scholar 

  35. Luitaud C, Laflamme C, Semlali A, Saidi S, Grenier G, Zakrzewski A, et al. Development of an engineering autologous palatal mucosa-like tissue for potential clinical applications. J Biomed Mater Res B Appl Biomater. 2007;83:554–61.

    CAS  PubMed  Google Scholar 

  36. Moharamzadeh K, Brook IM, Van Noort R, Scutt AM, Smith KG, Thornhill MH. Development, optimization and characterization of a full-thickness tissue engineered human oral mucosal model for biological assessment of dental biomaterials. J Mater Sci Mater Med. 2008;19:1793–801.

    CAS  PubMed  Google Scholar 

  37. Kinikoglu B, Auxenfans C, Pierrillas P, Justin V, Breton P, Burillon C, et al. Reconstruction of a full-thickness collagen-based human oral mucosal equivalent. Biomaterials. 2009;30:6418–25.

    CAS  PubMed  Google Scholar 

  38. Chapple CR, Macneil S. Tissue engineered oral mucosa for urethroplasty: past experience and future directions. J Urol. 2012;187:1533–4.

    CAS  PubMed  Google Scholar 

  39. Xie M, Xu Y, Song L, Wang J, Lv X, Zhang Y. Tissue-engineered buccal mucosa using silk fibroin matrices for urethral reconstruction in a canine model. J Surg Res 2013; pii: S0022-4804(13)02134-3.

  40. Lucier RN, Etienne O, Ferreira S, Garlick JA, Kugel G, Egles C. Soft-tissue alterations following exposure to tooth-whitening agents. J Periodontol. 2013;84:513–9.

    PubMed  Google Scholar 

  41. Moharamzadeh K, Franklin KL, Brook IM, van Noort R. Biologic assessment of antiseptic mouthwashes using a three-dimensional human oral mucosal model. J Periodontol. 2009;80:769–75.

    CAS  PubMed  Google Scholar 

  42. Kinikoglu B, Rovere MR, Haftek M, Hasirci V, Damour O. Influence of the mesenchymal cell source on oral epithelial development. J Tissue Eng Regen Med. 2012;6:245–52.

    CAS  PubMed  Google Scholar 

  43. Bucchieri F, Fucarino A, Marino Gammazza A, Pitruzzella A, Marciano V, Paderni C, et al. Medium-term culture of normal human oral mucosa: a novel three-dimensional model to study the effectiveness of drugs administration. Curr Pharm Des 2012;18:5421-30.

  44. Chai WL, Brook IM, Palmquist A, van Noort R, Moharamzadeh K. The biological seal of the implant-soft tissue interface evaluated in a tissue-engineered oral mucosal model. J R Soc Interface. 2012;9:3528–38.

    PubMed Central  PubMed  Google Scholar 

  45. Colley HE, Hearnden V, Jones AV, Weinreb PH, Violette SM, Macneil S, et al. Development of tissue-engineered models of oral dysplasia and early invasive oral squamous cell carcinoma. Br J Cancer. 2011;105:1582–92.

    PubMed Central  CAS  PubMed  Google Scholar 

  46. Yadev NP, Murdoch C, Saville SP, Thornhill MH. Evaluation of tissue engineered models of the oral mucosa to investigate oral candidiasis. Microb Pathog. 2011;50:278–85.

    CAS  PubMed  Google Scholar 

  47. Colley HE, Eves PC, Pinnock A, Thornhill MH, Murdoch C. Tissue-engineered oral mucosa to study radiotherapy-induced oral mucositis. Int J Radiat Biol. 2013;89:907–14.

    CAS  PubMed  Google Scholar 

  48. Cho KH, Ahn HT, Park KC, Chung JH, Kim SW, Sung MW, et al. Reconstruction of human hard-palate mucosal epithelium on deepidermized dermis. J Dermatol Sci. 2000;22:117–24.

    CAS  PubMed  Google Scholar 

  49. Ophof R, van Rheden RE, Von den Hoffa JW, Schalkwijk J, Kuijpers-Jagtman AM. Oral keratinocytes cultured on dermal matrices form a mucosa-like tissue. Biomaterials. 2002;23:3741–8.

    CAS  PubMed  Google Scholar 

  50. Bhargava S, Chapple CR, Bullock AJ, Layton C, MacNeil S. Tissue engineered buccal mucosa for substitution urethroplasty. BJU Int. 2004;93:807–11.

    CAS  PubMed  Google Scholar 

  51. Iida T, Takami Y, Yamaguchi R, Shimazaki S, Harii K. Development of a tissue-engineered human oral mucosa equivalent based on an acellular allogeneic dermal matrix: a preliminary report of clinical application to burn wounds. Scand J Plast Reconstr Surg Hand Surg. 2005;39:138–46.

    PubMed  Google Scholar 

  52. Izumi K, Takacs G, Terashi H, Feinberg SE. Ex vivo development of a composite human oral mucosal equivalent. J Oral Maxillofac Surg. 1999;57:571–7.

    CAS  PubMed  Google Scholar 

  53. Izumi K, Terashi H, Marcelo CL, Feinberg SE. Development and characterization of a tissue-engineered human oral mucosa equivalent produced in a serum-free culture system. J Dent Res. 2000;79:798–805.

    CAS  PubMed  Google Scholar 

  54. Yoshizawa M, Koyama T, Kojima T, Kato H, Ono Y, Saito C. Keratinocytes of tissue-engineered human oral mucosa promote re-epithelialization after intraoral grafting in athymic mice. J Oral Maxillofac Surg. 2012;70:1199–214.

    PubMed  Google Scholar 

  55. Hildebrand HC, Hakkinen L, Wiebe CB, Larjava HS. Characterization of organotypic keratinocyte cultures on deepithelialized bovine tongue mucosa. Histol Histopathol. 2002;17:151–63.

    CAS  PubMed  Google Scholar 

  56. Dang JM, Leong KW. Natural polymers for gene delivery and tissue engineering. Adv Drug Deliv Rev. 2006;58:487–99.

    CAS  PubMed  Google Scholar 

  57. Yannas IV, Burke JF. Design of an artificial skin. I. Basic design principles. J Biomed Mater Res. 1980;14:65–81.

    CAS  PubMed  Google Scholar 

  58. 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;14:107–32.

    CAS  PubMed  Google Scholar 

  59. Glowacki J, Mizuno S. Collagen scaffolds for tissue engineering. Biopolymers. 2008;89:338–44.

    CAS  PubMed  Google Scholar 

  60. Moharamzadeh K, Brook IM, van Noort R, Scutt AM, Thornhill MH. Tissue-engineered oral mucosa: a review of the scientific literature. J Dent Res. 2007;86:115–24.

    CAS  PubMed  Google Scholar 

  61. Claveau I, Mostefaoui Y, Rouabhia M. Basement membrane protein and matrix metalloproteinase deregulation in engineered human oral mucosa following infection with Candida albicans. Matrix Biol. 2004;23:477–86.

    CAS  PubMed  Google Scholar 

  62. Tardif F, Goulet JP, Zakrazewski A, Chauvin P, Rouabhia M. Involvement of interleukin-18 in the inflammatory response against oropharyngeal candidiasis. Med Sci Monit. 2004;10:239–49.

    Google Scholar 

  63. Kinikoglu B, Hemar J, Hasirci V, Breton P, Damour O. Feasibility of a porcine oral mucosa equivalent: a preclinical study. Artif Cell Blood Sub. 2012;40:271–4.

    CAS  Google Scholar 

  64. Terada M, Izumi K, Ohnuki H, Saito T, Kato H, Yamamoto M, et al. Construction and characterization of a tissue-engineered oral mucosa equivalent based on a chitosan-fish scale collagen composite. J Biomed Mater Res B Appl Biomater. 2012;100:1792–802.

    PubMed  Google Scholar 

  65. Bustos RH, Suesca E, Millán D, González JM, Fontanilla MR. Real-time quantification of proteins secreted by artificial connective tissue made from uni- or multidirectional collagen I scaffolds and oral mucosa fibroblasts. Anal Chem. 2014;86:2421–8.

    CAS  PubMed  Google Scholar 

  66. Peña I, Junquera LM, Meana A, García E, García V, De Vicente JC. In vitro engineering of complete autologous oral mucosa equivalents: characterization of a novel scaffold. J Periodontal Res. 2010;45:375–80.

    PubMed  Google Scholar 

  67. San Martin S, Alaminos M, Zorn TM, Sánchez-Quevedo MC, Garzón I, Rodriguez IA et al. The effects of fibrin and fibrin-agarose on the extracellular matrix profile of bioengineered oral mucosa. J Tissue Eng Regen Med 2013;7:10-9.

  68. Golinski PA, Gröger S, Herrmann JM, Bernd A, Meyle J. Oral mucosa model based on a collagen-elastin matrix. J Periodontal Res. 2011;46:704–11.

    CAS  PubMed  Google Scholar 

  69. Gunatillake PA, Adhikari R. Biodegradable synthetic polymers for tissue engineering. Eur Cell Mater. 2003;5:1–16.

    CAS  PubMed  Google Scholar 

  70. Rodríguez-Cabello JC, Prieto S, Reguera J, Arias FJ, Ribeiro A. Biofunctional design of elastin-like polymers for advanced applications in nanobiotechnology. J Biomater Sci Polymer Edn. 2007;18:269–86.

    Google Scholar 

  71. Rodríguez-Cabello JC, Martín L, Alonso M, Arias FJ, Testera AM. “Recombinamers” as advanced materials for the post-oil age. Polymer. 2009;50:5159–69.

    Google Scholar 

  72. Chilkoti A, Christensen T, MacKay JA. Stimulus responsive elastin biopolymers: applications in medicine and biotechnology. Curr Opin Chem Biol. 2006;10:652–7.

    PubMed Central  CAS  PubMed  Google Scholar 

  73. Ozturk N, Girotti A, Kose GT, Rodríguez-Cabello JC, Hasirci V. Dynamic cell culturing and its application to micropatterned, elastin-like protein-modified poly(N-isopropylacrylamide) scaffolds. Biomaterials. 2009;30:5417–26.

    CAS  PubMed  Google Scholar 

  74. Costa RR, Custódio CA, Arias FJ, Rodríguez-Cabello JC, Mano JF. Layer-by-layer assembly of chitosan and recombinant biopolymers into biomimetic coatings with multiple stimuli-responsive properties. Small. 2011;7:2640–9.

    CAS  PubMed  Google Scholar 

  75. Minato A, Ise H, Goto M, Akaike T. Cardiac differentiation of embryonic stem cells by substrate immobilization of insulin-like growth factor binding protein 4 with elastin-like polypeptides. Biomaterials. 2012;33:515–23.

    CAS  PubMed  Google Scholar 

  76. Ciofani G, Genchi GG, Liakos I, Athanassiou A, Mattoli V, Bandiera A. Human recombinant elastin-like protein coatings for muscle cell proliferation and differentiation. Acta Biomater. 2013;9:5111–21.

    CAS  PubMed  Google Scholar 

  77. Huang L, McMillan RA, Apkarian RP, Pourdeyhimi B, Conticello VP, Chaikof EL. Generation of synthetic elastin-mimetic small diameter fibers and fiber networks. Macromolecules. 2000;33:2989–97.

    CAS  Google Scholar 

  78. Martínez-Osorio H, Juárez-Campo M, Diebold Y, Girotti A, Alonso M, Arias FJ, et al. Genetically engineered elastin-like polymer as a substratum to culture cells from the ocular surface. Curr Eye Res. 2009;34:48–56.

    PubMed  Google Scholar 

  79. Costa RR, Testera AM, Arias FJ, Rodríguez-Cabello JC, Mano JF. Layer-by-layer film growth using polysaccharides and recombinant polypeptides: a combinatorial approach. J Phys Chem B. 2013;117:6839–48.

    CAS  PubMed  Google Scholar 

  80. Betre H, Ong SR, Guilak F, Chilkoti A, Fermor B, Setton LA. Chondrocytic differentiation of human adipose-derived adult stem cells in elastin-like polypeptide. Biomaterials. 2006;27:91–9.

    CAS  PubMed  Google Scholar 

  81. Martín L, Alonso M, Girotti A, Arias FJ, Rodríguez-Cabello JC. Synthesis and characterization of macroporous thermosensitive hydrogels from recombinant elastin-like polymers. Biomacromolecules. 2009;10:3015–22.

    PubMed  Google Scholar 

  82. Nettles DL, Haider MA, Chilkoti A, Setton LA. Neural network analysis identifies scaffold properties necessary for in vitro chondrogenesis in elastin-like polypeptide biopolymer scaffolds. Tissue Eng Part A. 2010;16:11–20.

    PubMed Central  CAS  PubMed  Google Scholar 

  83. Asai D, Xu D, Liu W, Garcia Quiroz F, Callahan DJ, Zalutsky MR, et al. Protein polymer hydrogels by in situ, rapid and reversible self-gelation. Biomaterials 2012;33:5451-8.

  84. Urry DW, Pattanaik A, Xu J, Woods TC, McPherson DT, Parker TM. Elastic protein-based polymers in soft tissue augmentation and generation. In: Polymers for tissue engineering. Brill Academic Publishers, The Netherlands (1998).

  85. Adams SB Jr, Shamji MF, Nettles DL, Hwang P, Setton LA. Sustained release of antibiotics from injectable and thermally responsive polypeptide depots. J Biomed Mater Res B Appl Biomater. 2009;90:67–74.

    PubMed Central  PubMed  Google Scholar 

  86. Garcia Y, Hemantkumar N, Collighan R, Griffin M, Rodriguez-Cabello JC, Pandit A. In vitro characterization of a collagen scaffold enzymatically cross-linked with a tailored elastin-like polymer. Tissue Eng Part A. 2009;15:887–99.

    CAS  PubMed  Google Scholar 

  87. Kinikoglu B, Rodríguez-Cabello JC, Damour O, Hasirci V. A smart bilayer scaffold of elastin-like recombinamer and collagen for soft tissue engineering. J Mater Sci Mater Med. 2011;22:1541–54.

    CAS  PubMed  Google Scholar 

  88. Kinikoglu B, Rodríguez-Cabello JC, Damour O, Hasirci V. The influence of elastin-like recombinant polymer on the self-renewing potential of a 3D tissue equivalent derived from human lamina propria fibroblasts and oral epithelial cells. Biomaterials. 2011;32:5756–64.

    CAS  PubMed  Google Scholar 

  89. Buckley CT, O’Kelly KU. Regular scaffold fabrication techniques for investigations in tissue engineering, Trinity Centre for Bioengineering & National Centre for Biomedical Engineering Science (2004).

  90. Weigel T, Schinkel G, Lendlein A. Design and preparation of polymeric scaffolds for tissue engineering. Expert Rev Med Devices. 2006;3:835–51.

    CAS  PubMed  Google Scholar 

  91. Chen G, Ushida T, Tateishi T. Scaffold design for tissue engineering. Macromol Biosci. 2002;2:67–77.

    CAS  Google Scholar 

  92. Freyman TM, Yannas IV, Gibson LJ. Cellular materials as porous scaffolds for tissue engineering. Progr Mater Sci. 2001;46:273–82.

    CAS  Google Scholar 

  93. 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.

    CAS  PubMed  Google Scholar 

  94. Madaghiele M, Sannino A, Yannas IV, Spector M. Collagen-based matrices with axially oriented pores. J Biomed Mater Res Part A. 2008;85A:757–67.

    CAS  Google Scholar 

  95. Nisbet DR, Forsythe JS, Shen W, Finkelstein DI, Horne MK. Review paper: a review of the cellular response on electrospun nanofibers for tissue engineering. J Biomater Appl. 2009;24:7–29.

    CAS  PubMed  Google Scholar 

  96. Matthews JA, Wnek GE, Simpson DG, Bowlin GL. Electrospinning of collagen nanofibers. Biomacromolecules. 2002;3:232–8.

    CAS  PubMed  Google Scholar 

  97. Tuzlakoglu K, Reis RL. Biodegradable polymeric fiber structures in tissue engineering. Tissue Eng Part B Rev. 2009;15:17–27.

    CAS  PubMed  Google Scholar 

  98. Powell HM, Supp DM, Boyce ST. Influence of electrospun collagen on wound contraction of engineered skin substitutes. Biomaterials. 2008;29:834–43.

    CAS  PubMed  Google Scholar 

  99. Rho KS, Jeong L, Lee G, Seo BM, Park YJ, Hong SD, et al. Electrospinning of collagen nanofibers: effects on the behavior of normal human keratinocytes and early-stage wound healing. Biomaterials. 2006;27:1452–61.

    CAS  PubMed  Google Scholar 

  100. Noh HK, Lee SW, Kim JM, Oh JE, Kim KH, Chung CP, et al. Electrospinning of chitin nanofibers: degradation behavior and cellular response to normal human keratinocytes and fibroblasts. Biomaterials. 2006;27:3934–44.

    CAS  PubMed  Google Scholar 

  101. 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.

    CAS  PubMed  Google Scholar 

  102. Yeo IS, Oh JE, Jeong L, Lee TS, Lee SJ, Park WH, et al. Collagen-based biomimetic nanofibrous scaffolds: preparation and characterization of collagen/silk fibroin bicomponent nanofibrous structures. Biomacromolecules. 2008;9:1106–16.

    CAS  PubMed  Google Scholar 

  103. Zhou Y, Yang D, Chen X, Xu Q, Lu F, Nie J. Electrospun water-soluble carboxyethyl chitosan/poly(vinyl alcohol) nanofibrous membrane as potential wound dressing for skin regeneration. Biomacromolecules. 2008;9:349–54.

    CAS  PubMed  Google Scholar 

  104. Duan B, Wu L, Yuan X, Hu Z, Li X, Zhang Y, et al. Hybrid nanofibrous membranes of PLGA/chitosan fabricated via an electrospinning array. J Biomed Mater Res A. 2007;83:868–78.

    PubMed  Google Scholar 

  105. Kim G, Kim W. Highly porous 3D nanofiber scaffold using an electrospinning technique. J Biomed Mater Res B Appl Biomater. 2007;81:104–10.

    PubMed  Google Scholar 

  106. Black AF, Hudon V, Damour O, Germain L, Auger FA. A novel approach for studying angiogenesis: a human skin equivalent with a capillary-like network. Cell Biol Toxicol. 1999;15:81–90.

    CAS  PubMed  Google Scholar 

  107. Wake MC, Patrick CW Jr, Mikos AG. Pore morphology effects on the fibrovascular tissue growth in porous polymer substrates. Cell Transplant. 1994;3:339–43.

    CAS  PubMed  Google Scholar 

  108. Hosseinkhani H, Hosseinkhani M, Khademhosseini A, Kobayashi H, Tabata Y. Enhanced angiogenesis through controlled release of basic fibroblast growth factor from peptide amphiphile for tissue regeneration. Biomaterials. 2006;27:5836–44.

    CAS  PubMed  Google Scholar 

  109. Sonis ST. The pathobiology of mucositis. Nat Rev Cancer. 2004;4:277–84.

    CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Medical Biology, School of Medicine, Acibadem University, 34742, Istanbul, Turkey

    Beste Kinikoglu

  2. Banque de Tissus et Cellules, Hospices Civils de Lyon, 69437, Lyon, France

    Odile Damour

  3. Department of Biological Sciences, BIOMATEN, METU CoE in Biomaterials and Tissue Engineering, 06800, Ankara, Turkey

    Vasif Hasirci

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  1. Beste Kinikoglu
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  2. Odile Damour
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  3. Vasif Hasirci
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Correspondence to Beste Kinikoglu.

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Kinikoglu, B., Damour, O. & Hasirci, V. Tissue engineering of oral mucosa: a shared concept with skin. J Artif Organs 18, 8–19 (2015). https://doi.org/10.1007/s10047-014-0798-5

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