Tissue engineering of skin and regenerative medicine for wound care

Abstract

ᅟ Engineering of biologic skin substitutes has progressed over time from individual applications of skin cells, or biopolymer scaffolds, to combinations of cells and scaffolds for treatment, healing, and closure of acute and chronic skin wounds. Skin substitutes may be categorized into three groups: acellular scaffolds, temporary substitutes containing allogeneic skin cells, and permanent substitutes containing autologous skin cells. Combined use of acellular dermal substitutes with permanent skin substitutes containing autologous cells has been shown to provide definitive wound closure in burns involving greater than 90% of the total body surface area. These advances have contributed to reduced morbidity and mortality from both acute and chronic wounds but, to date, have failed to replace all of the structures and functions of the skin. Among the remaining deficiencies in cellular or biologic skin substitutes are hypopigmentation, absence of stable vascular and lymphatic networks, absence of hair follicles, sebaceous and sweat glands, and incomplete innervation. Correction of these deficiencies depends on regulation of biologic pathways of embryonic and fetal development to restore the full anatomy and physiology of uninjured skin. Elucidation and integration of developmental biology into future models of biologic skin substitutes promises to restore complete anatomy and physiology, and further reduce morbidity from skin wounds and scar. This article offers a review of recent advances in skin cell thrapies and discusses the future prospects in cutaneous regeneration.

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References 146

1. 1.

   Finnerty CC, Capek K, Voigt C, Hundeshagen G, Cambiaso-Daniel J, Porter C, Sousse LE, El Ayadi A, Zapata-Sirvent R, Guillory A, et al. The P50 research center in perioperative sciences: how the investment by the National Institute of General Medical Sciences in Team Science has reduced post-burn mortality. J Trauma Acute Care Surg. 2017;83(3):532-542.

   Not in our library10.1097/ta.0000000000001644 (opens in a new tab)

2. 2.

   Warden GD, Saffle JR, Kravitz M. A two-stage technique for excision and grafting of burn wounds. J Trauma. 1982;22(2):98-103.

   Not in our library10.1097/00005373-198202000-00004 (opens in a new tab)

3. 3.

   Wood FM, Giles N, Stevenson A, Rea S, Fear M. Characterisation of the cell suspension harvested from the dermal epidermal junction using a ReCell(R) kit. Burns. 2012;38(1):44-51.

   Not in our library10.1016/j.burns.2011.03.001 (opens in a new tab)

4. 4.

   Green H, Kehinde O, Thomas J. Growth of human epidermal cells into multiple epithelia suitable for grafting. Proc Natl Acad Sci U S A. 1979;76:5665-5668.

   Not in our library10.1073/pnas.76.11.5665 (opens in a new tab)

5. 5.

   Boyce ST, Hansbrough JF. Biologic attachment, growth, and differentiation of cultured human epidermal keratinocytes on a graftable collagen and chondroitin-6-sulfate substrate. Surgery. 1988;103:421-431.

   Not in our library

6. 6.

   Falanga V, Sabolinski M. A bilayered living skin construct (APLIGRAF) accelerates complete closure of hard-to-heal venous ulcers. Wound Repair Regen. 1999;7(4):201-207.

   Not in our library10.1046/j.1524-475x.1999.00201.x (opens in a new tab)

7. 7.

   Griffiths M, Ojeh N, Livingstone R, Price R, Navsaria H. Survival of Apligraf in acute human wounds. Tissue Eng. 2004;10(7-8):1180-1195.

   Not in our library10.1089/ten.2004.10.1180 (opens in a new tab)

8. 8.

   Centanni JM, Straseski JA, Wicks A, Hank JA, Rasmussen CA, Lokuta MA, Schurr MJ, Foster KN, Faucher LD, Caruso DM, et al. StrataGraft skin substitute is well-tolerated and is not acutely immunogenic in patients with traumatic wounds: results from a prospective, randomized, controlled dose escalation trial. Ann Surg. 2011;253(4):672-683.

   Not in our library10.1097/sla.0b013e318210f3bd (opens in a new tab)

9. 9.

   Parenteau NL, Sabolinski M, Prosky S, Nolte C, Oleson M, Kriwet K, Bilbo P. Biological and physical factors influencing the successful engraftment of a cultured human skin substitute. Biotechnol Bioeng. 1996;523:3-14.

   Not in our library10.1002/(sici)1097-0290(19961005)52:1<3::aid-bit1>3.0.co;2-p (opens in a new tab)

10. 10.

    Alexander JW, MacMillan BG, Law E, Kittur DS. Treatment of severe burns with widely meshed skin autograft, and meshed skin allograft overlay. J Trauma. 1981;21(6):433-438.

    Not in our library

11. 11.

    Medina A, Riegel T, Nystad D, Tredget EE. Modified meek micrografting technique for wound coverage in extensive burn injuries. J Burn Care Res. 2016;37(5):305-313.

    Not in our library10.1097/bcr.0000000000000244 (opens in a new tab)

12. 12.

    Gallico Iii GG, O'Connor NE, Compton CC, Remensynder JP, Kehinde O, Green H. Cultured epithelial autografts for giant congenital nevi. Plast Reconstr Surg. 1989;84:1-9.

    Not in our library10.1097/00006534-198907000-00001 (opens in a new tab)

13. 13.

    Nikkhah D, Booth S, Tay S, Gilbert P, Dheansa B. Comparing outcomes of sheet grafting with 1:1 mesh grafting in patients with thermal burns: a randomized trial. Burns. 2015;41(2):257-264.

    Not in our library10.1016/j.burns.2014.07.023 (opens in a new tab)

14. 14.

    Compton CC, Warland G, Kratz G. Melanocytes in cultured epithelial grafts are depleted with serial subcultivation and cryopreservation: implications for clinical outcome. J Burn Care Rehabil. 1998;19(4):330-336.

    Not in our library10.1097/00004630-199807000-00011 (opens in a new tab)

15. 15.

    Harriger MD, Warden GD, Greenhalgh DG, Kagan RJ, Boyce ST. Pigmentation and microanatomy of skin regenerated from composite grafts of cultured cells and biopolymers applied to full-thickness burn wounds. Transplantation. 1995;59(5):702-707.

    Not in our library10.1097/00007890-199503150-00011 (opens in a new tab)

16. 16.

    Greenhalgh DG. A primer on pigmentation. J Burn Care Res. 2015;36(2):247-257.

    Not in our library10.1097/bcr.0000000000000224 (opens in a new tab)

17. 17.

    Heimbach D, Luterman A, Burke J, Cram A, Herndon D, Hunt J, Jordan M, McManus W, Solem L, Warden G, Zawacki B. Artificial dermis for major burns: a multi-center randomized clinical trial. Ann Surg. 1988;208(3):313–9.

    Not in our library10.1097/00000658-198809000-00008 (opens in a new tab)

18. 18.

    Atherton DD, Tang R, Jones I, Jawad M. Early excision and application of matriderm with simultaneous autologous skin grafting in facial burns. Plast Reconstr Surg. 2010;125(2):60e-61e.

    Not in our library10.1097/prs.0b013e3181c725e5 (opens in a new tab)

19. 19.

    Jansen LA, De CP, Guay NA, Lineaweaver WC, Shokrollahi K. The evidence base for the acellular dermal matrix AlloDerm: a systematic review. Ann Plast Surg. 2013;70(5):587-594.

    Not in our library10.1097/sap.0b013e31827a2d23 (opens in a new tab)

20. 20.

    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(2):269-274.

    Not in our library10.1097/bcr.0b013e318031a236 (opens in a new tab)

21. 21.

    Greenwood JE, Dearman BL. Split skin graft application over an integrating, biodegradable temporizing polymer matrix: immediate and delayed. J Burn Care Res. 2012;33(1):7-19.

    Not in our library10.1097/bcr.0b013e3182372be9 (opens in a new tab)

22. 22.

    Greenwood JE, Wagstaff MJ, Rooke M, Caplash Y. Reconstruction of extensive calvarial exposure after major burn injury in 2 stages using a biodegradable polyurethane matrix. Eplasty. 2016;16:e17.

    Not in our library

23. 23.

    Muangman P, Deubner H, Honari S, Heimbach DM, Engrav LH, Klein MB, Gibran NS. Correlation of clinical outcome of integra application with microbiologic and pathological biopsies. J Trauma. 2006;61(5):1212-1217.

    Not in our library10.1097/01.ta.0000195982.71400.84 (opens in a new tab)

24. 24.

    Heimbach DM, Warden GD, Luterman A, Jordan MH, Ozobia N, Ryan CM, Voigt DW, Hickerson WL, Saffle JR, DeClement FA, et al. Multicenter postapproval clinical trial of Integra dermal regeneration template for burn treatment. J Burn Care Rehabil. 2003;24(1):42-48.

    Not in our library10.1097/00004630-200301000-00009 (opens in a new tab)

25. 25.

    Branski LK, Herndon DN, Pereira C, Mlcak RP, Celis MM, Lee JO, Sanford AP, Norbury WB, Zhang XJ, Jeschke MG. Longitudinal assessment of Integra in primary burn management: a randomized pediatric clinical trial. Crit Care Med. 2007;35(11):2615-2623.

    Not in our library10.1097/01.ccm.0000285991.36698.e2 (opens in a new tab)

26. 26.

    Kopp J, Magnus NE, Rubben A, Merk HF, Pallua N. Radical resection of giant congenital melanocyte nevus and reconstruction with meek-graft covered integra dermal template. Dermatol Surg. 2003;29(6):653-657.

    Not in our library10.1046/j.1524-4725.2003.29157.x (opens in a new tab)

27. 27.

    Moiemen NS, Vlachou E, Staiano JJ, Thawy Y, Frame JD. Reconstructive surgery with Integra dermal regeneration template: histologic study, clinical evaluation, and current practice. Plast Reconstr Surg. 2006;117(7 Suppl):160S-174S.

    Not in our library10.1097/01.prs.0000222609.40461.68 (opens in a new tab)

28. 28.

    Herndon DN. Total burn care. 2012.

    Not in our library

29. 29.

    Kagan RJ, Robb EC, Plessinger RT. Human skin banking. Clin Lab Med. 2005;25(3):587-605.

    Not in our library10.1016/j.cll.2005.06.008 (opens in a new tab)

30. 30.

    Harris RP, Compton JB, Abstan S. Comparison of fresh, frozen, and lyophilized porcine skin as xenografts on burned patients. Burns. 1976;2:71-75.

    Not in our library10.1016/s0305-4179(76)80001-0 (opens in a new tab)

31. 31.

    Burkey B, Davis W, Glat PM. Porcine xenograft treatment of superficial partial-thickness burns in paediatric patients. J Wound Care. 2016;25(2):S10-S15.

    Not in our library10.12968/jowc.2016.25.sup2.s10 (opens in a new tab)

32. 32.

    Hermans MH. Porcine xenografts vs. (cryopreserved) allografts in the management of partial thickness burns: is there a clinical difference? Burns. 2014;40(3):408-415.

    Not in our library10.1016/j.burns.2013.08.020 (opens in a new tab)

33. 33.

    Schurr MJ, Foster KN, Lokuta MA, Rasmussen CA, Thomas-Virnig CL, Faucher LD, Caruso DM, len-Hoffmann BL. Clinical evaluation of NIKS-based bioengineered skin substitute tissue in complex skin defects: phase I/IIa clinical trial results. Adv Wound Care (New Rochelle). 2012;1(2):95-103.

    Not in our library10.1089/wound.2011.0343 (opens in a new tab)

34. 34.

    Sood R, Roggy D, Zieger M, Balledux J, Chaudhari S, Koumanis DJ, Mir HS, Cohen A, Knipe C, Gabehart K, et al. Cultured epithelial autografts for coverage of large burn wounds in eighty-eight patients: the Indiana University experience. J Burn Care Res. 2010;31(4):559-568.

    Not in our library10.1097/bcr.0b013e3181e4ca29 (opens in a new tab)

35. 35.

    Gravante G, Di Fede MC, Araco A, Grimaldi M, De AB, Arpino A, Cervelli V, Montone A. A randomized trial comparing ReCell system of epidermal cells delivery versus classic skin grafts for the treatment of deep partial thickness burns. Burns. 2007;33(8):966-972.

    Not in our library10.1016/j.burns.2007.04.011 (opens in a new tab)

36. 36.

    Duranceau L, Genest H, Bortoluzzi P, Moulin V, Auger FA, Germain L. Successful grafting of a novel autologous tissue-engineered skin substitutes (dermis and epidermis) on twelve burn patients. J Burn Care Res. 2014;35(3):S121.

    Not in our library

37. 37.

    Boyce ST, Warden GD. Principles and practices for treatment of cutaneous wounds with cultured skin substitutes. Am J Surg. 2002;183(4):445-456.

    Not in our library10.1016/s0002-9610(02)00813-9 (opens in a new tab)

38. 38.

    Hansbrough JF, Boyce ST, Cooper ML, Foreman TJ. Burn wound closure with cultured autologous keratinocytes and fibroblasts attached to a collagen-glycosaminoglycan substrate. JAMA. 1989;262(15):2125-2130.

    Not in our library10.1001/jama.1989.03430150093032 (opens in a new tab)

39. 39.

    Boyce ST, Simpson PS, Rieman MT, Warner PM, Yakuboff KP, Kevin BJ, Nelson JK, Fowler LA, Kagan RJ. Randomized, paired-site comparison of autologous engineered skin substitutes and split-thickness skin graft for closure of extensive, full-thickness burns. J Burn Care Res. 2017;38(2):61-70.

    Not in our library10.1097/bcr.0000000000000401 (opens in a new tab)

40. 40.

    Desai MH, Mlakar JM, McCauley RL, Abdullah KM, Rutan RL, Waymack JP, Robson MC, Herndon DN. Lack of long term durability of cultured keratinocyte burn wound coverage: a case report. J Burn Care Rehabil. 1991;12:540-545.

    Not in our library10.1097/00004630-199111000-00009 (opens in a new tab)

41. 41.

    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(4):395-401.

    Not in our library10.1016/j.burns.2006.01.008 (opens in a new tab)

42. 42.

    Sood R, Roggy DE, Zieger MJ, Nazim M, Hartman BC, Gibbs JT. A comparative study of spray keratinocytes and autologous meshed split-thickness skin graft in the treatment of acute burn injuries. Wounds. 2015;27(2):31-40.

    Not in our library

43. 43.

    Boyce ST, Medrano EE, Abdel-Malek ZA, Supp AP, Dodick JM, Nordlund JJ, Warden GD. Pigmentation and inhibition of wound contraction by cultured skin substitutes with adult melanocytes after transplantation to athymic mice. J Invest Dermat. 1993;100(4):360-365.

    Not in our library10.1111/1523-1747.ep12471822 (opens in a new tab)

44. 44.

    Bottcher-Haberzeth S, Klar AS, Biedermann T, Schiestl C, Meuli-Simmen C, Reichmann E, Meuli M. “Trooping the color”: restoring the original donor skin color by addition of melanocytes to bioengineered skin analogs. Pediatr Surg Intl. 2013;29(3):239-247.

    Not in our library10.1007/s00383-012-3217-0 (opens in a new tab)

45. 45.

    Duval C, Chagnoleau C, Pouradier F, Sextius P, Condom E, Bernerd F. Human skin model containing melanocytes: essential role of keratinocyte growth factor for constitutive pigmentation-functional response to alpha-melanocyte stimulating hormone and forskolin. Tissue Eng Part C Methods. 2012;18(12):947-957.

    Not in our library10.1089/ten.tec.2011.0676 (opens in a new tab)

46. 46.

    Supp DM, Wilson-Landy K, Boyce ST. Human dermal microvascular endothelial cells form vascular analogs in cultured skin substitutes after grafting to athymic mice. FASEB J. 2002;16(8):797-804.

    Not in our library10.1096/fj.01-0868com (opens in a new tab)

47. 47.

    Black AF, Berthod F, L'Heureux N, Germain L, Auger FA. In vitro reconstruction of a human capillary-like network in a tissue-engineered skin equivalent. FASEB J. 1998;12(13):1331-1340.

    Not in our library10.1096/fasebj.12.13.1331 (opens in a new tab)

48. 48.

    Tremblay PL, Hudon V, Berthod F, Germain L, Auger FA. Inosculation of tissue-engineered capillaries with the host’s vasculature in a reconstructed skin transplanted on mice. Am J Transplant. 2005;5(5):1002-1010.

    Not in our library10.1111/j.1600-6143.2005.00790.x (opens in a new tab)

49. 49.

    Bhowmick S, Scharnweber D, Koul V. Co-cultivation of keratinocyte-human mesenchymal stem cell (hMSC) on sericin loaded electrospun nanofibrous composite scaffold (cationic gelatin/hyaluronan/chondroitin sulfate) stimulates epithelial differentiation in hMSCs: in vitro study. Biomaterials. 2016;88:83-96.

    Not in our library10.1016/j.biomaterials.2016.02.034 (opens in a new tab)

50. 50.

    Klar AS, Biedermann T, Michalak K, Michalczyk T, Meuli-Simmen C, Scherberich A, Meuli M, Reichmann E. Human adipose mesenchymal cells inhibit melanocyte differentiation and the pigmentation of human skin via increased expression of TGF-beta1. J Invest Dermatol. 2017;137(12):2560-2569.

    Not in our library10.1016/j.jid.2017.06.027 (opens in a new tab)

51. 51.

    Huang S, Lu G, Wu Y, Jirigala E, Xu Y, Ma K, Fu X. Mesenchymal stem cells delivered in a microsphere-based engineered skin contribute to cutaneous wound healing and sweat gland repair. J Dermatol Sci. 2012;66(1):29-36.

    Not in our library10.1016/j.jdermsci.2012.02.002 (opens in a new tab)

52. 52.

    Morissette Martin P, Maux A, Laterreur V, Mayrand D, V LG, Moulin VJ, Fradette J. Enhancing repair of full-thickness excisional wounds in a murine model: impact of tissue-engineered biological dressings featuring human differentiated adipocytes. Acta Biomaterialia. 2015;22:39–49.

    Not in our library10.1016/j.actbio.2015.04.036 (opens in a new tab)

53. 53.

    Blais M, Parenteau-Bareil R, Cadau S, Berthod F. Concise review: tissue-engineered skin and nerve regeneration in burn treatment. Stem Cells Transl Med. 2013;2(7):545-551.

    Not in our library10.5966/sctm.2012-0181 (opens in a new tab)

54. 54.

    Sriwiriyanont P, Lynch KA, McFarland KL, Supp DM, Boyce ST. Characterization of hair follicle development in engineered skin substitutes. PLoS One. 2013;8(6):e65664.

    Not in our library10.1371/journal.pone.0065664 (opens in a new tab)

55. 55.

    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(6):1375-1378.

    Not in our library10.1038/jid.2011.34 (opens in a new tab)

56. 56.

    Agabalyan NA, Rosin NL, Rahmani W, Biernaskie J. Hair follicle dermal stem cells and skin-derived precursor cells: exciting tools for endogenous and exogenous therapies. Exp Dermatol. 2017;26(6):505-509.

    Not in our library10.1111/exd.13359 (opens in a new tab)

57. 57.

    Gledhill K, Guo Z, Umegaki-Arao N, Higgins CA, Itoh M, Christiano AM. Melanin transfer in human 3D skin equivalents generated exclusively from induced pluripotent stem cells. PLoS One. 2015;10(8):e0136713.

    Not in our library10.1371/journal.pone.0136713 (opens in a new tab)

58. 58.
    Generation of 3D Skin Equivalents Fully Reconstituted from Human Induced Pluripotent Stem Cells (iPSCs) · 2013

    No notice
59. 59.

    Boyce ST, Lloyd CM, Kleiner MC, Swope VB, Abdel-Malek Z, Supp DM. Restoration of cutaneous pigmentation by transplantation to mice of isogeneic human melanocytes in dermal-epidermal engineered skin substitutes. Pigment Cell Melanoma Res. 2017;30(6):531-540.

    Not in our library10.1111/pcmr.12609 (opens in a new tab)

60. 60.

    Zhang Y, Tomann P, Andl T, Gallant NM, Huelsken J, Jerchow B, Birchmeier W, Paus R, Piccolo S, Mikkola ML, et al. Reciprocal requirements for EDA/EDAR/NF-kappaB and Wnt/beta-catenin signaling pathways in hair follicle induction. Dev Cell. 2009;17(1):49-61.

    Not in our library10.1016/j.devcel.2009.05.011 (opens in a new tab)

61. 61.

    Morgan BA. The dermal papilla: an instructive niche for epithelial stem and progenitor cells in development and regeneration of the hair follicle. Cold Spring Harb Perspect Med. 2014;4(7):a015180.

    Not in our library10.1101/cshperspect.a015180 (opens in a new tab)

62. 62.

    Morgan JR, Barrandon Y, Green H, Mulligan RC. Expression of an exogenous growth hormone gene in transplantable human epidermal cells. Science. 1987;237:1476-1479.

    Not in our library10.1126/science.3629250 (opens in a new tab)

63. 63.

    Wilson JM, Birinyi LK, Salomon RN, Libby P, Callow AD, Mulligan RC. Genetically modified endothelial cells in the treatment of human diseases. Trans Assoc Am Physicians. 1989;102:139-147.

    Not in our library

64. 64.

    Selden RF, Skoskiewicz MJ, Howie KB, Russell PS, Goodman HM. Implantation of genetically engineered fibroblasts into mice: implications for gene therapy. Science. 1987;236(4802):714-718.

    Not in our library10.1126/science.3472348 (opens in a new tab)

65. 65.

    Clement F, Grockowiak E, Zylbersztejn F, Fossard G, Gobert S, Maguer-Satta V. Stem cell manipulation, gene therapy and the risk of cancer stem cell emergence. Stem Cell Investig. 2017;4:67.

    Not in our library10.21037/sci.2017.07.03 (opens in a new tab)

66. 66.

    White M, Whittaker R, Gandara C, Stoll EA. A guide to approaching regulatory considerations for lentiviral-mediated gene therapies. Hum Gene Ther Methods. 2017;28(4):163-176.

    Not in our library10.1089/hgtb.2017.096 (opens in a new tab)

67. 67.

    Bals R, Weiner DJ, Moscioni AD, Meegalla RL, Wilson JM. Augmentation of innate host defense by expression of a cathelicidin antimicrobial peptide. Infect Immun. 1999;67(11):6084-6089.

    Not in our library10.1128/iai.67.11.6084-6089.1999 (opens in a new tab)

68. 68.

    Comer AR, Rasmussen CA, Thomas-Virnig CL, Lokuta MA, Shaughnessy LM, Schlosser SJ, Johnston CE, Bauer RL, Cleven TD, Wieczorek NC, et al. Preclinical development and planned clinical evaluation of a human skin substitute engineered to secrete elevated levels of a host defense peptide. Proceedings of the Innovations in Wound Healing Conference. 2014; (abstract).

    Not in our library

69. 69.

    Siprashvili Z, Nguyen NT, Bezchinsky MY, Marinkovich MP, Lane AT, Khavari PA. Long-term type VII collagen restoration to human epidermolysis bullosa skin tissue. Hum Gene Ther. 2010;21(10):1299-1310.

    Not in our library10.1089/hum.2010.023 (opens in a new tab)

70. 70.

    Ortiz-Urda S, Lin Q, Green CL, Keene DR, Marinkovich MP, Khavari PA. Injection of genetically engineered fibroblasts corrects regenerated human epidermolysis bullosa skin tissue. J Clin Invest. 2003;111(2):251-255.

    Not in our library10.1172/jci200317193 (opens in a new tab)

71. 71.

    Gibson AL, Thomas-Virnig CL, Centanni JM, Schlosser SJ, Johnston CE, Van Winkle KF, Szilagyi A, He LK, Shankar R, Allen-Hoffmann BL. Nonviral human beta defensin-3 expression in a bioengineered human skin tissue: a therapeutic alternative for infected wounds. Wound Repair Regen. 2012;20(3):414-424.

    Not in our library10.1111/j.1524-475x.2012.00786.x (opens in a new tab)

72. 72.

    Komor AC, Badran AH, Liu DR. CRISPR-based technologies for the manipulation of eukaryotic genomes. Cell. 2017;168(1-2):20-36.

    Not in our library10.1016/j.cell.2016.10.044 (opens in a new tab)

73. 73.

    Go DE, Stottmann RW. The impact of CRISPR/Cas9-based genomic engineering on biomedical research and medicine. Curr Mol Med. 2016;16(4):343-352.

    Not in our library10.2174/1566524016666160316150847 (opens in a new tab)

74. 74.

    Peng R, Lin G, Li J. Potential pitfalls of CRISPR/Cas9-mediated genome editing. FEBS J. 2016;283(7):1218-1231.

    Not in our library10.1111/febs.13586 (opens in a new tab)

75. 75.

    Patra S, Young V. A review of 3D printing techniques and the future in biofabrication of bioprinted tissue. Cell Biochem Biophys. 2016;74(2):93-98.

    Not in our library10.1007/s12013-016-0730-0 (opens in a new tab)

76. 76.

    Lee V, Singh G, Trasatti JP, Bjornsson C, Xu X, Tran TN, Yoo SS, Dai G, Karande P. Design and fabrication of human skin by three-dimensional bioprinting. Tissue Engineering Part C Methods. 2014;20(6):473-484.

    Not in our library10.1089/ten.tec.2013.0335 (opens in a new tab)

77. 77.

    Cui X, Boland T. Human microvasculature fabrication using thermal inkjet printing technology. Biomaterials. 2009;30(31):6221-6227.

    Not in our library10.1016/j.biomaterials.2009.07.056 (opens in a new tab)

78. 78.

    Koch L, Deiwick A, Schlie S, Michael S, Gruene M, Coger V, Zychlinski D, Schambach A, Reimers K, Vogt PM, et al. Skin tissue generation by laser cell printing. Biotechnol Bioeng. 2012;109(7):1855-1863.

    Not in our library10.1002/bit.24455 (opens in a new tab)

79. 79.

    Cho HJ, Youn SW, Cheon SI, Kim TY, Hur J, Zhang SY, Lee SP, Park KW, Lee MM, Choi YS, et al. Regulation of endothelial cell and endothelial progenitor cell survival and vasculogenesis by integrin-linked kinase. Arterioscler Thromb Vasc Biol. 2005;25(6):1154-1160.

    Not in our library10.1161/01.atv.0000164312.20008.93 (opens in a new tab)

80. 80.

    Burke-Smith A, Collier J, Jones I. A comparison of non-invasive imaging modalities: Infrared thermography, spectrophotometric intracutaneous analysis and laser Doppler imaging for the assessment of adult burns. Burns. 2015;41(8):1695-1707.

    Not in our library10.1016/j.burns.2015.06.023 (opens in a new tab)

81. 81.

    Jaskille AD, Ramella-Roman JC, Shupp JW, Jordan MH, Jeng JC. Critical review of burn depth assessment techniques: part II. Review of laser doppler technology. J Burn Care Res. 2010;31(1):151-157.

    Not in our library10.1097/bcr.0b013e3181c7ed60 (opens in a new tab)

82. 82.

    Ida T, Iwazaki H, Kawaguchi Y, Kawauchi S, Ohkura T, Iwaya K, Tsuda H, Saitoh D, Sato S, Iwai T. Burn depth assessments by photoacoustic imaging and laser Doppler imaging. Wound Repair Regen. 2016;24(2):349-355.

    Not in our library10.1111/wrr.12374 (opens in a new tab)

83. 83.

    Farrar E, Pujji O, Jeffery S. Three-dimensional wound mapping software compared to expert opinion in determining wound area. Burns. 2017;43(8):1736-1741.

    Not in our library10.1016/j.burns.2017.05.015 (opens in a new tab)

84. 84.

    Bailey JK, Burkes SA, Visscher MO, Whitestone J, Kagan RJ, Yakuboff KP, Warner P, Randall Wickett R. Multimodal quantitative analysis of early pulsed-dye laser treatment of scars at a pediatric burn hospital. Dermatol Surg. 2012;38(9):1490-1496.

    Not in our library10.1111/j.1524-4725.2012.02451.x (opens in a new tab)

85. 85.

    Serup J, Jemed GBE, Grove GL. Handbook of non-invasive methods and the skin, 2nd edn. CRC Press, Inc.: Boca Raton; 2006.

    Not in our library

86. 86.

    US Food and Drug Administration. Guidance for industry: guidance for human somatic cell therapy and gene therapy. Federal Register. 1998;63:36413.

    Not in our library

87. 87.

    US Food and Drug Administration. Guidance for industry: chronic cutaneous ulcer and burn wounds - developing products for treatment. Federal Register. 2006;65(125):39912.

    Not in our library

88. 88.

    American Society for Testing and Materials. Standard guide for preservation of tissue engineered medical products. In., Report No.: F 2386-04. 2007.

    Not in our library

89. 89.

    American Society for Testing and Materials. Standard guide for classification of therapeutic skin substitutes. In., Report No.: F 2311-08. 2009.

    Not in our library

90. 90.

    US Food and Drug Administration. Guidance for industry: how to write a request for designation. 2011.

    Not in our library

91. 91.

    Witten CM, McFarland RD, Simek SL. Concise review: the U.S. Food and Drug Administration and Regenerative Medicine. Stem Cells Transl Med. 2015;4(12):1495-1499.

    Not in our library10.5966/sctm.2015-0098 (opens in a new tab)

92. 92.

    US Food and Drug Administration. Expanded access for medical devices: compassionate use. 2014.

    Not in our library

93. 93.

    US Food and Drug Administration. Expanded access (Compassionate use). 2017.

    Not in our library

94. 94.

    US Food and Drug Administration. 21st century cures act. 2017.

    Not in our library

95. 95.

    US Food and Drug Administration. Fast track. 2017.

    Not in our library

96. 96.

    US Food and Drug Administration. Breakthrough therapy. 2017.

    Not in our library

97. 97.

    US Food and Drug Administration. Accelerated approval. 2017.

    Not in our library

98. 98.

    US Food and Drug Administration. Priority review. 2017.

    Not in our library

99. 99.

    Boyce ST. Design principles for composition and performance of cultured skin substitutes. Burns. 2001;27(5):523-533.

    Not in our library10.1016/s0305-4179(01)00019-5 (opens in a new tab)

100. 100.

     Boyce ST, Supp DM, Albanna MZ, Holmes JH. Biologic skin substitutes. Skin tissue engineering and regenerative medicine. 2016;211-238.

     Not in our library

101. 101.

     Lohana P, Hassan S, Watson SB. Integra in burns reconstruction: our experience and report of an unusual immunological reaction. Ann Burns Fire Disasters. 2014;27(1):17-21.

     Not in our library

102. 102.

     Ellis CV, Kulber DA. Acellular dermal matrices in hand reconstruction. Plast Reconstr Surg. 2012;130(5 Suppl 2):256S-269S.

     Not in our library10.1097/prs.0b013e318265a5cf (opens in a new tab)

103. 103.
     Biologic and synthetic skin substitutes: An overview · 2010

     No notice
104. 104.

     DeVries HJC, Mekkes JR, Middelkoop E, Hinrichs WLJ, Wildevuur CHR. Dermal substitutes for full-thickness wounds in one-stage grafting model. Wound Repair Regen. 1993;1:244-252.

     Not in our library10.1046/j.1524-475x.1993.10410.x (opens in a new tab)

105. 105.

     Myers SR, Partha VN, Soranzo C, Price RD, Navsaria HA. Hyalomatrix: a temporary epidermal barrier, hyaluronan delivery, and neodermis induction system for keratinocyte stem cell therapy. Tissue Eng. 2007;13(11):2733-2741.

     Not in our library10.1089/ten.2007.0109 (opens in a new tab)

106. 106.

     Greenwood JE, Dearman BL. Comparison of a sealed, polymer foam biodegradable temporizing matrix against Integra(R) dermal regeneration template in a porcine wound model. J Burn Care Res. 2012;33(1):163-173.

     Not in our library10.1097/bcr.0b013e318233fac1 (opens in a new tab)

107. 107.

     May SR, DeClement F. Skin banking. Part I. Procurement of transplantable cadaveric allograft skin for burn wound coverage. J Burn Care Rehabil. 1981;2:7-23.

     Not in our library10.1097/00004630-198101000-00003 (opens in a new tab)

108. 108.

     Griffiths CEM, Nickoloff BJ. Keratinocyte intercellular adhesion molecule-1 (ICAM-1) expression precedes dermal T lymphocyte infiltration in allergic contact dermatitis (Rhus dermatitis). Am J Pathol. 1989;135:1045-1053.

     Not in our library

109. 109.

     Carlson M, Faria K, Shamis Y, Leman J, Ronfard V, Garlick J. Epidermal stem cells are preserved during commercial-scale manufacture of a bilayered, living cellular construct (Apligraf(R)). Tissue Eng Part A. 2011;17(3-4):487-493.

     Not in our library10.1089/ten.tea.2010.0268 (opens in a new tab)

110. 110.

     Schurr MJ, Foster KN, Centanni JM, Comer AR, Wicks A, Gibson AL, Thomas-Virnig CL, Schlosser SJ, Faucher LD, Lokuta MA, et al. Phase I/II clinical evaluation of StrataGraft: a consistent, pathogen-free human skin substitute. J Trauma. 2009;66(3):866-873.

     Not in our library10.1097/ta.0b013e31819849d6 (opens in a new tab)

111. 111.

     Frykberg RG, Marston WA, Cardinal M. The incidence of lower-extremity amputation and bone resection in diabetic foot ulcer patients treated with a human fibroblast-derived dermal substitute. Adv Skin Wound Care. 2015;28(1):17-20.

     Not in our library10.1097/01.asw.0000456630.12766.e9 (opens in a new tab)

112. 112.

     Harding K, Sumner M, Cardinal M. A prospective, multicentre, randomised controlled study of human fibroblast-derived dermal substitute (Dermagraft) in patients with venous leg ulcers. Intnl Wound J. 2013;10(2):132-137.

     Not in our library10.1111/iwj.12053 (opens in a new tab)

113. 113.

     Gallico Iii GG, O'Connor NE, Compton CC, Kehinde O, Green H. Permanent coverage of large burn wounds with autologous cultured human epithelium. N Engl J Med. 1984;311:448-451.

     Not in our library10.1056/nejm198408163110706 (opens in a new tab)

114. 114.

     Campanella SD, Rapley P, Ramelet AS. A randomised controlled pilot study comparing Mepitel ® and SurfaSoft ® on paediatric donor sites treated with Recell ®. Burns. 2011;37(8):1334-1342.

     Not in our library10.1016/j.burns.2011.04.019 (opens in a new tab)

115. 115.

     Boa O, Cloutier CB, Genest H, Labbe R, Rodrigue B, Soucy J, Roy M, Arsenault F, Ospina CE, Dube N, et al. Prospective study on the treatment of lower-extremity chronic venous and mixed ulcers using tissue-engineered skin substitute made by the self-assembly approach. Adv Skin Wound Care. 2013;26(9):400-409.

     Not in our library10.1097/01.asw.0000433102.48268.2a (opens in a new tab)

116. 116.

     Boyce ST, Kagan RJ, Greenhalgh DG, Warner P, Yakuboff KP, Palmieri T, Warden GD. Cultured skin substitutes reduce requirements for harvesting of skin autograft for closure of excised, full-thickness burns. J Trauma. 2006;60(4):821-829.

     Not in our library10.1097/01.ta.0000196802.91829.cc (opens in a new tab)

117. 117.

     Elsholz F, Harteneck C, Muller W, Friedland K. Calcium--a central regulator of keratinocyte differentiation in health and disease. Eur J Dermatol. 2014;24(6):650-661.

     Not in our library10.1684/ejd.2014.2452 (opens in a new tab)

118. 118.

     Boyce ST, Ham RG. Calcium-regulated differentiation of normal human epidermal keratinocytes in chemically defined clonal culture and serum-free serial culture. J Invest Dermatol. 1983;81(1 Suppl):33s-40s.

     Not in our library10.1111/1523-1747.ep12540422 (opens in a new tab)

119. 119.

     Rice RH, Durbin-Johnson BP, Ishitsuka Y, Salemi M, Phinney BS, Rocke DM, Roop DR. Proteomic analysis of loricrin knockout mouse epidermis. J Proteome Res. 2016;15(8):2560-2566.

     Not in our library10.1021/acs.jproteome.6b00108 (opens in a new tab)

120. 120.

     Wikramanayake TC, Stojadinovic O, Tomic-Canic M. Epidermal Differentiation in Barrier Maintenance and Wound Healing. Adv Wound Care (New Rochelle). 2014;3(3):272-280.

     Not in our library10.1089/wound.2013.0503 (opens in a new tab)

121. 121.

     Feingold KR, Elias PM. Role of lipids in the formation and maintenance of the cutaneous permeability barrier. Biochim Biophys Acta. 2014;1841(3):280-294.

     Not in our library10.1016/j.bbalip.2013.11.007 (opens in a new tab)

122. 122.

     Ponec M, Weerheim A, Kempenaar J, Mulder A, Gooris GS, Bouwstra J, Mommaas AM. The formation of competent barrier lipids in reconstructed human epidermis requires the presence of vitamin C. J Invest Dermatol. 1997;109(3):348-355.

     Not in our library10.1111/1523-1747.ep12336024 (opens in a new tab)

123. 123.

     Haass NK, Smalley KS, Li L, Herlyn M. Adhesion, migration and communication in melanocytes and melanoma. Pigment Cell Res. 2005;18(3):150-159.

     Not in our library10.1111/j.1600-0749.2005.00235.x (opens in a new tab)

124. 124.

     Kramer IJ, Kramer IJ. Integrins, cell survival, and cell proliferation. Cell Signalling. 2016;681-693.

     Not in our library

125. 125.

     Kippenberger S, Hofmann M, Zoller N, Thaci D, Muller J, Kaufmann R, Bernd A. Ligation of beta4 integrins activates PKB/Akt and ERK1/2 by distinct pathways-relevance of the keratin filament. Biochim Biophys Acta. 2010;1803(8):940-950.

     Not in our library10.1016/j.bbamcr.2010.03.009 (opens in a new tab)

126. 126.

     Ohyama M, Zheng Y, Paus R, Stenn KS. The mesenchymal component of hair follicle neogenesis: background, methods and molecular characterization. Exp Dermatol. 2009;19(2):89-99.

     Not in our library10.1111/j.1600-0625.2009.00935.x (opens in a new tab)

127. 127.

     Chueh SC, Lin SJ, Chen CC, Lei M, Wang LM, Widelitz R, Hughes MW, Jiang TX, Chuong CM. Therapeutic strategy for hair regeneration: hair cycle activation, niche environment modulation, wound-induced follicle neogenesis, and stem cell engineering. Expert Opin Biol Ther. 2013;13(3):377-391.

     Not in our library10.1517/14712598.2013.739601 (opens in a new tab)

128. 128.

     Kiso M, Tanaka S, Saba R, Matsuda S, Shimizu A, Ohyama M, Okano HJ, Shiroishi T, Okano H, Saga Y. The disruption of Sox21-mediated hair shaft cuticle differentiation causes cyclic alopecia in mice. Proc Natl Acad Sci USA. 2009;106(23):9292-9297.

     Not in our library10.1073/pnas.0808324106 (opens in a new tab)

129. 129.

     Driskell RR, Clavel C, Rendl M, Watt FM. Hair follicle dermal papilla cells at a glance. J Cell Sci. 2011;124(Pt 8):1179-1182.

     Not in our library10.1242/jcs.082446 (opens in a new tab)

130. 130.
     WNT10A mutation causes ectodermal dysplasia by impairing progenitor cell proliferation and KLF4-mediated differentiation · 2017

     No notice
131. 131.

     Niemann C, Horsley V. Development and homeostasis of the sebaceous gland. Semin Cell Dev Biol. 2012;23(8):928-936.

     Not in our library10.1016/j.semcdb.2012.08.010 (opens in a new tab)

132. 132.

     McNairn AJ, Doucet Y, Demaude J, Brusadelli M, Gordon CB, Uribe-Rivera A, Lambert PF, Bouez C, Breton L, Guasch G. TGFbeta signaling regulates lipogenesis in human sebaceous glands cells. BMC Dermatol. 2013;13:2.

     Not in our library10.1186/1471-5945-13-2 (opens in a new tab)

133. 133.

     Lu C, Fuchs E. Sweat gland progenitors in development, homeostasis, and wound repair. Cold Spring Harb Perspect Med. 2014;4(2):a015222.

     Not in our library10.1101/cshperspect.a015222 (opens in a new tab)

134. 134.

     Zeng B, Xiao X, Li S, Lu H, Lu J, Zhu L, Yu D, Zhao W: Eight mutations of three genes (EDA, EDAR, and WNT10A) identified in seven hypohidrotic ectodermal dysplasia patients. Genes. 2016 7(9); epub. doi: 10.3390/genes7090065. PMID: 27657131.

     Not in our library10.3390/genes7090065 (opens in a new tab)

135. 135.

     Cui CY, Kunisada M, Esibizione D, Douglass EG, Schlessinger D. Analysis of the temporal requirement for eda in hair and sweat gland development. J Invest Dermatol. 2009;129(4):984-993.

     Not in our library10.1038/jid.2008.318 (opens in a new tab)

136. 136.

     Adameyko I, Lallemend F, Aquino JB, Pereira JA, Topilko P, Muller T, Fritz N, Beljajeva A, Mochii M, Liste I, et al. Schwann cell precursors from nerve innervation are a cellular origin of melanocytes in skin. Cell. 2009;139(2):366-379.

     Not in our library10.1016/j.cell.2009.07.049 (opens in a new tab)

137. 137.

     Cichorek M, Wachulska M, Stasiewicz A, Tyminska A. Skin melanocytes: biology and development. Postepy Dermatol Alergol. 2013;30(1):30-41.

     Not in our library10.5114/pdia.2013.33376 (opens in a new tab)

138. 138.

     Aoki Y, Saint-Germain N, Gyda M, Magner-Fink E, Lee YH, Credidio C, Saint-Jeannet JP. Sox10 regulates the development of neural crest-derived melanocytes in Xenopus. Dev Biol. 2003;259(1):19-33.

     Not in our library10.1016/s0012-1606(03)00161-1 (opens in a new tab)

139. 139.

     Kaucka M, Adameyko I. Non-canonical functions of the peripheral nerve. Exp Cell Res. 2014;321(1):17-24.

     Not in our library10.1016/j.yexcr.2013.10.004 (opens in a new tab)

140. 140.

     Biedermann T, Klar AS, Bottcher-Haberzeth S, Schiestl C, Reichmann E, Meuli M. Tissue-engineered dermo-epidermal skin analogs exhibit de novo formation of a near natural neurovascular link 10 weeks after transplantation. Pediatr Surg Int. 2014;30(2):165-172.

     Not in our library10.1007/s00383-013-3446-x (opens in a new tab)

141. 141.

     Francois M, Koopman P, Beltrame M. SoxF genes: key players in the development of the cardio-vascular system. Int J Biochem Cell Biol. 2010;42(3):445-448.

     Not in our library10.1016/j.biocel.2009.08.017 (opens in a new tab)

142. 142.

     Wat JJ, Wat MJ. Sox7 in vascular development: review, insights and potential mechanisms. Int J Dev Biol. 2014;58(1):1-8.

     Not in our library10.1387/ijdb.130323mw (opens in a new tab)

143. 143.

     Bruderer M, Alini M, Stoddart MJ. Role of HOXA9 and VEZF1 in endothelial biology. J Vasc Res. 2013;50(4):265-278.

     Not in our library10.1159/000353287 (opens in a new tab)

144. 144.

     Janani C, Ranjitha Kumari BD. PPAR gamma gene - A review. Diabetes Metab Syndr. 2015;9(1):46-50.

     Not in our library10.1016/j.dsx.2014.09.015 (opens in a new tab)

145. 145.

     Kang S, Kong X, Rosen ED. Adipocyte-specific transgenic and knockout models. Methods Enzymol. 2014;537:1-16.

     Not in our library10.1016/b978-0-12-411619-1.00001-x (opens in a new tab)

146. 146.

     Harms M, Seale P. Brown and beige fat: development, function and therapeutic potential. Nat Med. 2013;19(10):1252-1263.

     Not in our library10.1038/nm.3361 (opens in a new tab)

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