Design and fabrication of human skin by three-dimensional bioprinting

Tissue Engineering - Part C: Methods

Volumn 20, Issue 6, 2014, Pages 473-484

  Lee, Vivian ^a,b   Singh, Gurtej ^b,c   Trasatti, John P ^b,d   Bjornsson, Chris ^e   Xu, Xiawei ^f   Tran, Thanh Nga ^g   Yoo, Seung Schik ^h   Dai, Guohao ^a,b   Karande, Pankaj ^b,c  

^a RENSSELAER POLYTECHNIC INSTITUTE   (United States)

^b RENSSELAER POLYTECHNIC INSTITUTE   (United States)

^c Rensselaer Polytechnic Institute   (United States)

^d Research Rensselaer Polytechnic Institute   (United States)

^e Neural Stem Cell Institute   (United States)

^f UNIVERSITY OF PENNSYLVANIA   (United States)

^g MASSACHUSETTS GENERAL HOSPITAL   (United States)

^h HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; CELLS; DATA MINING; HISTOLOGY; PHYSIOLOGICAL MODELS; TISSUE;

AIR LIQUID INTERFACES; AUTOLOGOUS GRAFTS; EPIDERMAL LAYERS; IN-VIVO HUMAN SKIN; REPRODUCIBILITIES; SKIN ENGINEERING; THREE-DIMENSIONAL BIOPRINTING; TOPICAL FORMULATIONS;

TISSUE ENGINEERING;

COLLAGEN; NERVE CELL ADHESION MOLECULE;

ARTICLE; BIOPRINTING; CELL DENSITY; CELL DIFFERENTIATION; CELL INTERACTION; CELL INVASION; CELL PROLIFERATION; CELL SUSPENSION; CELL VIABILITY; DERMIS; EPIDERMIS; EXTRACELLULAR MATRIX; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; IN VIVO STUDY; KERATINOCYTE; MONOLAYER CULTURE; PRIORITY JOURNAL; SKIN; SKIN FIBROBLAST; SKINFOLD THICKNESS; THREE DIMENSIONAL BIOPRINTING; TISSUE ENGINEERING; TISSUE STRUCTURE; ARTIFICIAL SKIN; BIOPROSTHESIS; CELL CULTURE; CELL SURVIVAL; COCULTURE; CYTOLOGY; DEVICES; FIBROBLAST; GROWTH, DEVELOPMENT AND AGING; ORGAN CULTURE TECHNIQUE; PHYSIOLOGY; PROCEDURES; THREE DIMENSIONAL PRINTING;

BIOPROSTHESIS; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; COCULTURE TECHNIQUES; FIBROBLASTS; HUMANS; KERATINOCYTES; ORGAN CULTURE TECHNIQUES; PRINTING, THREE-DIMENSIONAL; SKIN; SKIN, ARTIFICIAL; TISSUE ENGINEERING;

EID: 84901016012     PISSN: 19373384     EISSN: 19373392     Source Type: Journal    
DOI: 10.1089/ten.tec.2013.0335     Document Type: Article

References (50)

1. Bos, J.D., and Meinardi, M.H. The 500 dalton rule for theskin penetration of chemical compounds and drugs. ExpDermatol 9, 165, 2000.
2. Bouwstra, J.A. The skin, a well organized membrane. ColloidsSurf A 123, 403, 1997.
3. Karande, P., and Mitragotri, S. Transcutaneous immunization:an overview of advantages, disease targets, vaccines,and delivery technologies. In: Prausnitz, J.M., Doherty, M.F.,and Segalman, M.A., eds. Ann Rev Chem Biomol Eng 1, 175,2010.
4. Adams, D.C., and Ramsey, M.L. Grafts in dermatologicsurgery: review and update on full-and split-thickness skingrafts, free cartilage grafts, and composite grafts. DermatolSurg 31, 1055, 2005.
5. Hierner, R., Degreef, H., Vranckx, J.J., Garmyn, M., Massage,P., and van Brussel, M. Skin grafting and wound healing-the "dermato-plastic team approach". Clin Dermatol 23, 343,2005.
6. MacFarlane, D.F. Current techniques in skin grafting.Adv Dermatol 22, 125, 2006.
7. Orgill, D.P. Excision and skin grafting of thermal burns.N Engl J Med 360, 893, 2009.
8. Karande, P., Arora, A., Pham, T.K., Stevens, D., Wojicki, A.,and Mitragotri, S. Transcutaneous immunization usingcommon chemicals. J Control Release 138, 134, 2009.
9. Karande, P., Jain, A., Arora, A., Ho, M.J., and Mitragotri, S.Synergistic effects of chemical enhancers on skin permeability:a case study of sodium lauroylsarcosinate and sorbitanmonolaurate. Eur J Pharmaceut Sci 31, 1, 2007.
10. Karande, P., Jain, A., Ergun, K., Kispersky, V., andMitragotri, S. Design principles of chemical penetration enhancersfor transdermal drug delivery. Proc Natl Acad SciUSA 102, 4688, 2005.
11. Karande, P., Jain, A., and Mitragotri, S. Discovery of transdermalpenetration enhancers by high-throughput screening.Nat Biotechnol 22, 192, 2004.
12. Karande, P., and Mitragotri, S. High throughput screening oftransdermal formulations. Pharmaceut Res 19, 655, 2002.
13. Adler, S., Basketter, D., Creton, S., Pelkonen, O., vanBenthem, J., Zuang, V., Andersen, K.E., Angers-Loustau, A.,Aptula, A., Bal-Price, A., Benfenati, E., Bernauer, U., Bessems,J., Bois, F.Y., Boobis, A., Brandon, E., Bremer, S., Broschard,T., Casati, S., Coecke, S., Corvi, R., Cronin, M., Daston, G.,Dekant, W., Felter, S., Grignard, E., Gundert-Remy, U., Heinonen,T., Kimber, I., Kleinjans, J., Komulainen, H., Kreiling,R., Kreysa, J., Leite, S.B., Loizou, G., Maxwell, G., Mazzatorta,P., Munn, S., Pfuhler, S., Phrakonkham, P., Piersma, A., Poth,A., Prieto, P., Repetto, G., Rogiers, V., Schoeters, G., Schwarz,M., Serafimova, R., Tahti, H., Testai, E., van Delft, J., vanLoveren, H., Vinken, M., Worth, A., and Zaldivar, J.-M. Alternative(non-animal) methods for cosmetics testing: currentstatus and future prospects-2010. Arch Toxicol 85, 367, 2011.
14. Ali, N., Chu, C.C., Karagiannis, P., Di Meglio, P., Skowera,A., Napolitano, L., Barinaga, G., Grys, K., Sharif-Paghaleh,E., Karagiannis, S.N., Peakman, M., Lombardi, G., andNestle, F.O. A novel skin-resident vitamin D-3-induciblehuman dendritic cell playing a critical role in tissue ho-meostasis and immunoregulation, as demonstrated in humanizedmouse models of disease. Br J Dermatol 166,e19, 2012.
15. Aloor, H., Peredo, C., Hofland, H., Smith, S.H., Therrien, J.,and Cote-Sierra, J. A new model for evaluating topicaltreatments for th17 mediated diseases using ex vivo humanskin. J Invest Dermatol 133, S3, 2013.
16. Kuechler, S., Henkes, D., Eckl, K.-M., Ackermann, K., Plendl,J., Korting, H.-C., Hennies, H.-C., and Schaefer-Korting, M.Hallmarks of atopic skin mimicked in vitro by means of askin disease model based on flg knock-down. Altern LabAnim 39, 471, 2011.
17. Semlin, L., Schaefer-Korting, M., Borelli, C., and Korting,H.C. In vitro models for human skin disease. Drug DiscovToday 16, 132, 2011.
18. Shevchenko, R.V., James. S.L., and James, S.E. A review oftissue-engineered skin bioconstructs available for skin reconstruction.J R Soc Interface 7, 229, 2010.
19. Wood, F.M., Kolybaba, M.L., and Allen, P. The use of culturedepithelial autograft in the treatment of major burnwounds: eleven years of clinical experience. Burns 32, 538,2006.
20. Macneil, S. Progress and opportunities for tissue-engineeredskin. Nature 445, 874, 2007.
21. Morikawa, N., Kitagawa, T., and Tomihata, K. Assessmentof the in vitro skin irritation of chemicals using the vitrolifeskin-human skin model. AATEX 14, 417, 2007.
22. Netzaff, F., Lehr, C.M., Wertz, P.W., and Schaefer, U.F. Thehuman epidermis models episkin (r), skinethic (r) and epiderm(r): an evaluation of morphology and their suitabilityfor testing phototoxicity, irritancy, corrosivity, and substancetransport. Eur J Pharmaceut Biopharmaceut 60, 167,2005.
23. Netzlaff, F., Kaca, M., Bock, U., Haltner-Ukomadu, E.,Meiers, P., Lehr, C.M., and Schaefer, U.F. Permeability of thereconstructed human epidermis model episkin (r) in comparisonto various human skin preparations. Eur J PharmaceutBiopharmaceut 66, 127, 2007.
24. Schafer-Korting, M., Bock, U., Diembeck, W., Duesing, H.J.,Gamer, A., Haltner-Ukomadu, E., Hoffmann, C., Kaca, M.,Kamp, H., Kersen, S., Kietzmann, M., Korting, H.C.,Krachter, H.U., Lehr, C.M., Liebsch, M., Mehling, A.,Mueller-Goymann, C., Netzlaff, F., Niedorf, F., Rubbelke,M.K., Schafer, U., Schmidt, E., Schreiber, S., Spielmann, H.,Vuia, A., and Weimer, M. The use of reconstructed humanepidermis for skin absorption testing: results of the validationstudy. Altern Lab Anim 36, 161, 2008.
25. Fransson, J., Heffler, L.C., Linder, M.T., and Scheynius, A.Culture of human epidermal langerhans cells in a skinequivalent. Br J Dermatol 139, 598, 1998.
26. Regnier, M., Patwardhan, A., Scheynius, A., and Schmidt, R.Reconstructed human epidermis composed of keratinocytes,melanocytes and langerhans cells. Med Biol Eng Comput 36,821, 1998.
27. Auxenfans, C., Fradette, J., Lequeux, C., Germain, L.,Kinikoglu, B., Bechetoille, N., Braye, F., Auger, F.A., andDamour, O. Evolution of three dimensional skin equivalentmodels reconstructed in vitro by tissue engineering. Eur JDermatol 19, 107, 2009.
28. Gangatirkar, P., Paquet-Fifield, S., Li, A., Rossi, R., and Kaur,P. Establishment of 3d organotypic cultures using humanneonatal epidermal cells. Nat Protoc 2, 178, 2007.
29. Souto, L.R., Rehder, J., Vassallo, J., Cintra, M.L., Kraemer,M.H., and Puzzi, M.B. Model for human skin reconstructedin vitro composed of associated dermis and epidermis. SaoPaulo Med J 124, 71, 2006.
30. Mironov, V., Visconti, R.P., Kasyanov, V., Forgacs, G.,Drake, C.J., and Markwald, R.R. Organ printing: tissuespheroids as building blocks. Biomaterials 30, 2164, 2009.
31. Mironov, V., Boland, T., Trusk, T., Forgacs, G., andMarkwald, R.R. Organ printing: computer-aided jet-based3d tissue engineering. Trends Biotechnol 21, 157, 2003.
32. Norotte, C., Marga, F.S., Niklason, L.E., and Forgacs, G.Scaffold-free vascular tissue engineering using bioprinting.Biomaterials 30, 5910, 2009.
33. Roth, E.A., Xu, T., Das, M., Gregory, C., Hickman, J.J., andBoland, T. Inkjet printing for high-throughput cell patterning.Biomaterials 25, 3707, 2004.
34. Xu, T., Jin, J., Gregory, C., Hickman, J.J., and Boland, T.Inkjet printing of viable mammalian cells. Biomaterials 26,93, 2005.
35. Bettinger, C.J., Weinberg, E.J., Kulig, K.M., Vacanti, J.P., Wang,Y.D., Borenstein, J.T., and Langer, R. Three-dimensionalmicrofluidic tissue-engineering scaffolds using a flexible biodegradablepolymer. Adv Mater 18, 165, 2006.
36. Borenstein, J.T., Weinberg, E.J., Orrick, B.K., Sundback, C.,Kaazempur-Mofrad, M.R., and Vacanti, J.P. Microfabricationof three-dimensional engineered scaffolds. Tissue Eng 13,1837, 2007.
37. Cooke, M.N., Fisher, J.P., Dean, D., Rimnac, C., and Mikos,A.G. Use of stereolithography to manufacture critical-sized3d biodegradable scaffolds for bone ingrowth. J BiomedMater Res Part B 64B, 65, 2003.
38. Dhariwala, B., Hunt, E., and Boland, T. Rapid prototypingof tissue-engineering constructs, using photopolymerizablehydrogels and stereolithography. Tissue Eng 10, 1316,2004.
39. Golden, A.P., and Tien, J. Fabrication of microfluidic hydrogelsusing molded gelatin as a sacrificial element. LabChip 7, 720, 2007.
40. Melchels, F.P., Grijpma, D., and Feijen, J. Photo-crosslinkingof functionalised lactide oligomers for the fabrication of osteochondraltissue engineering scaffolds. J Control Release116, e98, 2006.
41. Lee, W., Debasitis, J.C., Lee, V.K., Lee, J.H., Fischer, K.,Edminster, K., Park, J.K., and Yoo, S.S. Multi-layered cultureof human skin fibroblasts and keratinocytes throughthree-dimensional freeform fabrication. Biomaterials 30,1587, 2009.
42. Lee, W., Pinckney, J., Lee, V., Lee, J.H., Fischer, K., Polio, S.,Park, J.K., and Yoo, S.S. Three-dimensional bioprinting of ratembryonic neural cells. Neuroreport 20, 798, 2009.
43. Lee, W., Lee, V., Polio, S., Keegan, P., Lee, J.H., Fischer, K.,Park, J.K., and Yoo, S.S. On-demand three-dimensionalfreeform fabrication of multi-layered hydrogel scaffold withfluidic channels. Biotechnol Bioeng 105, 1178, 2010.
44. Zhao, L.L., Lee, V.K., Yoo, S.S., Dai, G.H., and Intes, X.The integration of 3-d cell printing and mesoscopic fluorescencemolecular tomography of vascular constructswithin thick hydrogel scaffolds. Biomaterials 33, 5325,2012.
45. Lee, Y.-B., Polio, S., Lee, W., Dai, G., Menon, L., Carroll, R.S.,and Yoo, S.-S. Bio-printing of collagen and vegf-releasingfibrin gel scaffolds for neural stem cell culture. Exp Neurol 223, 645, 2010.
46. Prunieras, M., Regnier, M., and Woodley, D. Methods forcultivation of keratinocytes with an air-liquid interface.J Invest Dermatol 81, 28s, 1983.
47. Lademann, J., Otberg, N., Richter, H., Meyer, L., Audring,H., Teichmann, A., Thomas, S., Knü ttel, A., and Sterry, W.Application of optical non-invasive methods in skin physiology:a comparison of laser scanning microscopy and opticalcoherent tomography with histological analysis. SkinRes Technol 13, 119, 2007.
48. Pontiggia, L., Klar, A., Boettcher-Haberzeth, S., Biedermann,T., Meuli, M., and Reichmann, E. Optimizing in vitro cultureconditions leads to a significantly shorter production time of human dermo-epidermal skin substitutes. Pediatr Surg Int29, 249, 2013.
49. Yang, J., Meyer, M., Mueller, A.-K., Boehm, F., Grose, R.,Dauwalder, T., Verrey, F., Kopf, M., Partanen, J., Bloch, W.,Ornitz, D.M., and Werner, S. Fibroblast growth factor receptors1 and 2 in keratinocytes control the epidermal barrier andcutaneous homeostasis. J Cell Biol 188, 935, 2010.
50. Yannas, I.V., Lee, E., Orgill, D.P., Skrabut, E.M., andMurphy, G.F. Synthesis and characterization of a modelextracellular matrix that induces partial regeneration ofadult mammalian skin. Proc Natl Acad Sci USA 86,933, 1989.