Unraveling barrier properties of three different in-house human skin equivalents

Tissue Engineering - Part C: Methods

Volumn 18, Issue 1, 2012, Pages 1-11

  Thakoersing, Varsha S ^a   Gooris, Gerrit S ^a   Mulder, Aat ^a   Rietveld, Marion ^b   El Ghalbzouri, Abdoelwaheb ^b   Bouwstra, Joke A ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; FATTY ACIDS; LIPIDS; MORPHOLOGY;

BARRIER FUNCTIONS; BARRIER PROPERTIES; COLLAGEN MODELS; DIFFERENTIATION MARKERS; FIBROBLAST-DERIVED MATRIX; FREE FATTY ACID; HUMAN SKIN; INTERCELLULAR REGIONS; LIPID COMPOSITION; STRATUM CORNEUM; THREE-DIMENSIONAL CULTURE MODEL; UPPER LAYER;

THREE DIMENSIONAL;

COLLAGEN TYPE 1; CYTOKERATIN 16; INVOLUCRIN; LIPID; PROTEIN PRECURSOR;

ARTICLE; ARTIFICIAL SKIN; BIOLOGICAL MODEL; BIOSYNTHESIS; CELL DIFFERENTIATION; CHEMISTRY; CYTOLOGY; FIBROBLAST; HUMAN; IMMUNOHISTOCHEMISTRY; INFRARED SPECTROSCOPY; KERATINOCYTE; METABOLISM; METHODOLOGY; PATHOLOGY; PERMEABILITY; SKIN; TISSUE ENGINEERING; TRANSMISSION ELECTRON MICROSCOPY;

CELL DIFFERENTIATION; COLLAGEN TYPE I; FIBROBLASTS; HUMANS; IMMUNOHISTOCHEMISTRY; KERATIN-16; KERATINOCYTES; LIPIDS; MICROSCOPY, ELECTRON, TRANSMISSION; MODELS, BIOLOGICAL; PERMEABILITY; PROTEIN PRECURSORS; SKIN; SKIN, ARTIFICIAL; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; TISSUE ENGINEERING;

EID: 84855371944     PISSN: 19373384     EISSN: 19373392     Source Type: Journal    
DOI: 10.1089/ten.tec.2011.0175     Document Type: Article

References (51)

1. Brusselaers, N., Pirayesh, A., Hoeksema, H., Richters, C.D., Verbelen, J., Beele, H., Blot, S.I., and Monstrey, S. Skin replacement in burn wounds. J Trauma 68, 490, 2010.
2. Shakespeare, P.G. The role of skin substitutes in the treatment of burn injuries. Clin Dermatol 23, 413, 2005.
3. Supp, D.M., and Boyce, S.T. Engineered skin substitutes: practices and potentials. Clin Dermatol 23, 403, 2005.
4. Alepee, N., Tornier, C., Robert, C., Amsellem, C., Roux, M.H., Doucet, O., Pachot, J., Meloni, M., and de Brugerolle de Fraissinette, A. A catch-up validation study on reconstructed human epidermis (SkinEthic RHE) for full replacement of the Draize skin irritation test. Toxicol In Vitro 24, 257, 2009.
5. Gibbs, S. In vitro irritation models and immune reactions. Skin Pharmacol Physiol 22, 103, 2009.
6. Netzlaff, F., Lehr, C.M., Wertz, P.W., and Schaefer, U.F. The human epidermis models EpiSkin, SkinEthic and EpiDerm: an evaluation of morphology and their suitability for testing phototoxicity, irritancy, corrosivity, and substance transport. Eur J Pharm Biopharm 60, 167, 2005.
7. El Ghalbzouri, A., Siamari, R., Willemze, R., and Ponec, M. Leiden reconstructed human epidermal model as a tool for the evaluation of the skin corrosion and irritation potential according to the ECVAM guidelines. Toxicol In Vitro 22, 1311, 2008.
8. Carlson, M.W., Alt-Holland, A., Egles, C., and Garlick, J.A. Three-dimensional tissue models of normal and diseased skin. Curr Protoc Cell Biol Chapter 19, Unit 19.9, 2008.
9. Engelhart, K., El Hindi, T., Biesalski, H.K., and Pfitzner, I. In vitro reproduction of clinical hallmarks of eczematous dermatitis in organotypic skin models. Arch Dermatol Res 297, 1, 2005.
10. Garlick, J.A. Engineering skin to study human disease-tissue models for cancer biology and wound repair. Adv Biochem Eng Biotechnol 103, 207, 2007.
11. Mildner, M., Jin, J., Eckhart, L., Kezic, S., Gruber, F., Barresi, C., Stremnitzer, C., Buchberger, M., Mlitz, V., Ballaun, C., Sterniczky, B., Fodinger, D., and Tschachler, E. Knockdown of filaggrin impairs diffusion barrier function and increases UV sensitivity in a human skin model. J Invest Dermatol 130, 2286, 2010.
12. Boelsma, E., Gibbs, S., Faller, C., and Ponec, M. Characterization and comparison of reconstructed skin models: morphological and immunohistochemical evaluation. Acta Derm Venereol 80, 82, 2000.
13. El-Ghalbzouri, A., Gibbs, S., Lamme, E., Van Blitterswijk, C.A., and Ponec, M. Effect of fibroblasts on epidermal regeneration. Br J Dermatol 147, 230, 2002.
14. Ponec, M., Boelsma, E., Weerheim, A., Mulder, A., Bouwstra, J., and Mommaas, M. Lipid and ultrastructural characterization of reconstructed skin models. Int J Pharm 203, 211, 2000.
15. El Ghalbzouri, A., Lamme, E., and Ponec, M. Crucial role of fibroblasts in regulating epidermal morphogenesis. Cell Tissue Res 310, 189, 2002.
16. Boehnke, K., Mirancea, N., Pavesio, A., Fusenig, N.E., Boukamp, P., and Stark, H.J. Effects of fibroblasts and microenvironment on epidermal regeneration and tissue function in long-term skin equivalents. Eur J Cell Biol 86, 731, 2007.
17. Stark, H.J., Boehnke, K., Mirancea, N., Willhauck, M.J., Pavesio, A., Fusenig, N.E., and Boukamp, P. Epidermal homeostasis in long-term scaffold-enforced skin equivalents. J Investig Dermatol Symp Proc 11, 93, 2006.
18. Bouwstra, J., Pilgram, G., Gooris, G., Koerten, H., and Ponec, M. New aspects of the skin barrier organization. Skin Pharmacol Appl Skin Physiol 14 Suppl 1, 52, 2001.
19. White, S.H., Mirejovsky, D., and King, G.I. Structure of lamellar lipid domains and corneocyte envelopes of murine stratum corneum. An X-ray diffraction study. Biochemistry 27, 3725, 1988.
20. McIntosh, T.J., Stewart, M.E., and Downing, D.T. X-ray diffraction analysis of isolated skin lipids: reconstitution of intercellular lipid domains. Biochemistry 35, 3649, 1996.
21. Bouwstra, J.A., Gooris, G.S., van der Spek, J.A., and Bras, W. Structural investigations of human stratum corneum by small-angle X-ray scattering. J Invest Dermatol 97, 1005, 1991.
22. Bouwstra, J.A., Gooris, G.S., Dubbelaar, F.E., and Ponec, M. Phase behavior of lipid mixtures based on human ceramides: coexistence of crystalline and liquid phases. J Lipid Res 42, 1759, 2001.
23. Goldsmith, L.A., and Baden, H.P. Uniquely oriented epidermal lipid. Nature 225, 1052, 1970.
24. Damien, F., and Boncheva, M. The extent of orthorhombic lipid phases in the stratum corneum determines the barrier efficiency of human skin in vivo. J Invest Dermatol 130, 611, 2010.
25. Batheja, P., Song, Y., Wertz, P., and Michniak-Kohn, B. Effects of growth conditions on the barrier properties of a human skin equivalent. Pharm Res 26, 1689, 2009.
26. Schmook, F.P., Meingassner, J.G., and Billich, A. Comparison of human skin or epidermis models with human and animal skin in in-vitro percutaneous absorption. Int J Pharm 215, 51, 2001.
27. Netzlaff, F., Kaca, M., Bock, U., Haltner-Ukomadu, E., Meiers, P., Lehr, C.M., and Schaefer, U.F. Permeability of the reconstructed human epidermis model Episkin in comparison to various human skin preparations. Eur J Pharm Biopharm 66, 127, 2007.
28. Schafer-Korting, M., Bock, U., Diembeck, W., Dusing, 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., Muller-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 human epidermis for skin absorption testing: results of the validation study. Altern Lab Anim 36, 161, 2008.
29. Asbill, C., Kim, N., El-Kattan, A., Creek, K., Wertz, P., and Michniak, B. Evaluation of a human bio-engineered skin equivalent for drug permeation studies. Pharm Res 17, 1092, 2000.
30. Ackermann, K., Borgia, S.L., Korting, H.C., Mewes, K.R., and Schafer-Korting, M. The Phenion full-thickness skin model for percutaneous absorption testing. Skin Pharmacol Physiol 23, 105, 2010.
31. Marjukka Suhonen, T., Pasonen-Seppanen, S., Kirjavainen, M., Tammi, M., Tammi, R., and Urtti, A. Epidermal cell culture model derived from rat keratinocytes with permeability characteristics comparable to human cadaver skin. Eur J Pharm Sci 20, 107, 2003.
32. Zghoul, N., Fuchs, R., Lehr, C.M., and Schaefer, U.F. Reconstructed skin equivalents for assessing percutaneous drug absorption from pharmaceutical formulations. Altex 18, 103, 2001.
33. Gibbs, S., Vicanova, J., Bouwstra, J., Valstar, D., Kempenaar, J., and Ponec, M. Culture of reconstructed epidermis in a defined medium at 33 degrees C shows a delayed epidermal maturation, prolonged lifespan and improved stratum corneum. Arch Dermatol Res 289, 585, 1997.
34. Kennedy, A.H., Golden, G.M., Gay, C.L., Guy, R.H., Francoeur, M.L., and Mak, V.H. Stratum corneum lipids of human epidermal keratinocyte air-liquid cultures: implications for barrier function. Pharm Res 13, 1162, 1996.
35. Ponec, M., Weerheim, A., Kempenaar, J., Mulder, A., Gooris, G.S., Bouwstra, J., and Mommaas, A.M. The formation of competent barrier lipids in reconstructed human epidermis requires the presence of vitamin C. J Invest Dermatol 109, 348, 1997.
36. Pappinen, S., Hermansson, M., Kuntsche, J., Somerharju, P., Wertz, P., Urtti, A., and Suhonen, M. Comparison of rat epidermal keratinocyte organotypic culture (ROC) with intact human skin: lipid composition and thermal phase be-havior of the stratum corneum. Biochim Biophys Acta 1778, 824, 2008.
37. Bouwstra, J.A., Gooris, G.S., Weerheim, A., Kempenaar, J., and Ponec, M. Characterization of stratum corneum structure in reconstructed epidermis by X-ray diffraction. J Lipid Res 36, 496, 1995.
38. El Ghalbzouri, A., Commandeur, S., Rietveld, M.H., Mulder, A.A., and Willemze, R. Replacement of animal-derived collagen matrix by human fibroblast-derived dermal matrix for human skin equivalent products. Biomaterials 30, 71, 2009.
39. Bouwstra, J.A., Groenink, H.W., Kempenaar, J.A., Romeijn, S.G., and Ponec, M. Water distribution and natural moisturizer factor content in human skin equivalents are regulated by environmental relative humidity. J Invest Dermatol 128, 378, 2008.
40. Thakoersing, V.S., Ponec, M., and Bouwstra, J.A. Generation of human skin equivalents under submerged conditionsmimicking the in utero environment. Tissue Eng Part A 16, 1433, 2009.
41. De Jager, M., Groenink, W., Bielsa i Guivernau, R., Andersson, E., Angelova, N., Ponec, M., and Bouwstra, J. A novel in vitro percutaneous penetration model: evaluation of barrier properties with p-aminobenzoic acid and two of its derivatives. Pharm Res 23, 951, 2006.
42. Bligh, E.G., and Dyer, W.J. A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37, 911, 1959.
43. Motta, S., Monti, M., Sesana, S., Caputo, R., Carelli, S., and Ghidoni, R. Ceramide composition of the psoriatic scale. Biochim Biophys Acta 1182, 147, 1993.
44. Masukawa, Y., Narita, H., Shimizu, E., Kondo, N., Sugai, Y., Oba, T., Homma, R., Ishikawa, J., Takagi, Y., Kitahara, T., Takema, Y., and Kita, K. Characterization of overall ceramide species in human stratum corneum. J Lipid Res 49, 1466, 2008.
45. Caussin, J., Gooris, G.S., Janssens, M., and Bouwstra, J.A. Lipid organization in human and porcine stratum corneum differs widely, while lipid mixtures with porcine ceramides model human stratum corneum lipid organization very closely. Biochim Biophys Acta 1778, 1472, 2008.
46. Cheng, T., Tjabringa, G.S., van Vlijmen-Willems, I.M., Hitomi, K., van Erp, P.E., Schalkwijk, J., and Zeeuwen, P.L. The cystatin M/E-controlled pathway of skin barrier formation: expression of its key components in psoriasis and atopic dermatitis. Br J Dermatol 161, 253, 2009.
47. Bouwstra, J.A., Gooris, G.S., Bras, W., and Talsma, H. Small angle X-ray scattering: possibilities and limitations in characterization of vesicles. Chem Phys Lipids 64, 83, 1993.
48. Janssens, M., Gooris, G.S., and Bouwstra, J.A. Infrared spectroscopy studies ofmixtures preparedwith synthetic ceramides varying in head group architecture: coexistence of liquid and crystalline phases. Biochim Biophys Acta 1788, 732, 2009.
49. Groen, D., Poole, D.S., Gooris, G.S., and Bouwstra, J.A. Is an orthorhombic lateral packing and a proper lamellar organization important for the skin barrier function? Biochim Biophys Acta 1808, 1529, 2011.
50. Gooris, G.S., and Bouwstra, J.A. Infrared spectroscopic study of stratum corneum model membranes prepared from human ceramides, cholesterol, and fatty acids. Biophys J 92, 2785, 2007.
51. Mak, V.H., Cumpstone, M.B., Kennedy, A.H., Harmon, C.S., Guy, R.H., and Potts, R.O. Barrier function of human keratinocyte cultures grown at the air-liquid interface. J Invest Dermatol 96, 323, 1991.