Lowered humidity produces human epidermal equivalents with enhanced barrier properties

Tissue Engineering - Part C: Methods

Volumn 21, Issue 1, 2015, Pages 15-22

  Sun, Richard ^a   Celli, Anna ^a,b   Crumrine, Debra ^a,b   Hupe, Melanie ^a,b   Adame, Lillian C ^a   Pennypacker, Sally D ^a,b   Park, Kyungho ^a   Uchida, Yoshikazu ^a,b   Feingold, Kenneth R ^a   Elias, Peter M ^a,b   Ilic, Dusko ^c   Mauro, Theodora M ^a,b  

^a SAN FRANCISCO VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

LIPID BILAYERS; REPAIR;

BARRIER PROPERTIES; ENVIRONMENTAL HUMIDITIES; EPIDERMAL BARRIER; GLUCOSYLCERAMIDE SYNTHASE; HUMAN EPIDERMIS; HUMAN KERATINOCYTE; PERMEABILITY BARRIERS; TRANSEPIDERMAL WATER LOSS;

SKIN;

ABC TRANSPORTER A12; CALCIUM; CALCIUM ION; CERAMIDE GLUCOSYLTRANSFERASE; CLAUDIN 1; CYCLIC AMP; CYTOKERATIN 1; CYTOKERATIN 10; PROTEIN ZO1; UVOMORULIN; ION; PROTEIN;

ARTICLE; CELL STRUCTURE; ELECTRON MICROSCOPY; EPIDERMIS; HUMAN; HUMAN CELL; HUMIDITY; IN VITRO STUDY; KERATINOCYTE; PERMEABILITY BARRIER; PH; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SKIN PERMEABILITY; SKIN WATER LOSS; UPREGULATION; WESTERN BLOTTING; CELL CULTURE; CYTOLOGY; GENE EXPRESSION REGULATION; GROWTH, DEVELOPMENT AND AGING; MALE; METABOLISM; NEWBORN; PHYSIOLOGY; ULTRASTRUCTURE;

CELLS, CULTURED; EPIDERMIS; GENE EXPRESSION REGULATION; HUMANS; HUMIDITY; INFANT, NEWBORN; IONS; MALE; PROTEINS;

EID: 84913618901     PISSN: 19373384     EISSN: 19373392     Source Type: Journal    
DOI: 10.1089/ten.tec.2014.0065     Document Type: Article

References (53)

1. Furuse, M., Hata, M., Furuse, K., Yoshida, Y., Haratake, A., Sugitani, Y., Noda, T., Kubo, A., and Tsukita, S. Claudin-based tight junctions are crucial for the mammalian epidermal barrier: a lesson from claudin-1-deficient mice. J Cell Biol 156, 1099, 2002.
2. Celli, A., Zhai, Y., Jiang, Y.J., Crumrine, D., Elias, P.M., Feingold, K.R., and Mauro, T.M. Tight junction properties change during epidermis development. Exp Dermatol 21, 798, 2012.
3. Tunggal, J.A., Helfrich, I., Schmitz, A., Schwarz, H., Gunzel, D., Fromm, M., Kemler, R., Krieg, T., and Niessen, C.M. E-cadherin is essential for in vivo epidermal barrier function by regulating tight junctions. EMBO J 24, 1146, 2005.
4. Komuves, L.G., Hanley, K., Jiang, Y., Katagiri, C., Elias, P.M., Williams, M.L., and Feingold, K.R. Induction of selected lipid metabolic enzymes and differentiation-linked structural proteins by air exposure in fetal rat skin explants. J Invest Dermatol 112, 303, 1999.
5. Elias, P.M., Nau, P., Hanley, K., Cullander, C., Crumrine, D., Bench, G., Sideras-Haddad, E., Mauro, T., Williams, M.L., and Feingold, K.R. Formation of the epidermal calcium gradient coincides with key milestones of barrier ontogenesis in the rodent. J Invest Dermatol 110, 399, 1998.
6. Hachem, J.P., Crumrine, D., Fluhr, J., Brown, B.E., Feingold, K.R., and Elias, P.M. pH directly regulates epidermal permeability barrier homeostasis, and stratum corneum integrity/cohesion. J Invest Dermatol 121, 345, 2003.
7. Menon, G.K., Grayson, S., and Elias, P.M. Ionic calcium reservoirs in mammalian epidermis: ultrastructural localization by ion-capture cytochemistry. J Invest Dermatol 84, 508, 1985.
8. Vicanova, J., Boelsma, E., Mommaas, A.M., Kempenaar, J.A., Forslind, B., Pallon, J., Egelrud, T., Koerten, H.K., and Ponec, M. Normalization of epidermal calcium distribution profile in reconstructed human epidermis is related to improvement of terminal differentiation and stratum corneum barrier formation. J Invest Dermatol 111, 97, 1998.
9. Behne, M.J., Sanchez, S., Barry, N.P., Kirschner, N., Meyer, W., Mauro, T.M., Moll, I., and Gratton, E. Major translocation of calcium upon epidermal barrier insult: imaging and quantification via FLIM/Fourier vector analysis. Arch Dermatol Res 303, 103, 2011.
10. Hennings, H., Michael, D., Cheng, C., Steinert, P., Holbrook, K., and Yuspa, S.H. Calcium regulation of growth and differentiation of mouse epidermal cells in culture. Cell 19, 245, 1980.
11. Menon, G.K., Price, L.F., Bommannan, B., Elias, P.M., and Feingold, K.R. Selective obliteration of the epidermal calcium gradient leads to enhanced lamellar body secretion. J Invest Dermatol 102, 789, 1994.
12. Ohman, H., and Vahlquist, A. In vivo studies concerning a pH gradient in human stratum corneum and upper epidermis. Acta Derm Venereol 74, 375, 1994.
13. Vaccaro, A.M., Muscillo, M., and Suzuki, K. Characterization of human glucosylsphingosine glucosyl hydrolase and comparison with glucosylceramidase. Eur J Biochem 146, 315, 1985.
14. Bowser, P.A., and Gray, G.M. Sphingomyelinase in pig and human epidermis. J Invest Dermatol 70, 331, 1978.
15. Ponec, M., Wauben-Penris, P.J., Burger, A., Kempenaar, J., and Bodde, H.E. Nitroglycerin and sucrose permeability as quality markers for reconstructed human epidermis. Skin Pharmacol 3, 126, 1990.
16. 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.
17. Simonetti, O., Hoogstraate, A.J., Bialik, W., Kempenaar, J.A., Schrijvers, A.H., Bodde, H.E., and Ponec, M. Visualization of diffusion pathways across the stratum corneum of native and in-vitro-reconstructed epidermis by confocal laser scanning microscopy. Arch Dermatol Res 287, 465, 1995.
18. 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.
19. 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.
20. 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.
21. Thakoersing, V.S., Gooris, G.S., Mulder, A., Rietveld, M., El Ghalbzouri, A., and Bouwstra, J.A. Unraveling barrier properties of three different in-house human skin equivalents. Tissue Eng Part C Methods 18, 1, 2012.
22. Williams, M.L., Hanley, K., Elias, P.M., and Feingold, K.R. Ontogeny of the epidermal permeability barrier. J Investig Dermatol Symp Proc 3, 75, 1998.
23. Hanley, K., Jiang, Y., Elias, P.M., Feingold, K.R., and Williams, M.L. Acceleration of barrier ontogenesis in vitro through air exposure. Pediatr Res 41, 293, 1997.
24. Prunieras, M., Regnier, M., and Woodley, D. Methods for cultivation of keratinocytes with an air-liquid interface. J Invest Dermatol 81, 28s, 1983.
25. Agren, J., Sjors, G., and Sedin, G. Ambient humidity influences the rate of skin barrier maturation in extremely preterm infants. J Pediatr 148, 613, 2006.
26. Conner, J.M., Soll, R.F., and Edwards, W.H. Topical ointment for preventing infection in preterm infants. Cochrane Database Syst Rev CD001150, 2004.
27. 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.
28. Boyce, S.T., and Williams, M.L. Lipid supplemented medium induces lamellar bodies and precursors of barrier lipids in cultured analogues of human skin. J Invest Dermatol 101, 180, 1993.
29. Vicanova, J., Weerheim, A.M., Kempenaar, J.A., and Ponec, M. Incorporation of linoleic acid by cultured human keratinocytes. Arch Dermatol Res 291, 405, 1999.
30. Rosdy, M., and Clauss, L.C. Terminal epidermal differentiation of human keratinocytes grown in chemically defined medium on inert filter substrates at the air-liquid interface. J Invest Dermatol 95, 409, 1990.
31. Ponec, M., Gibbs, S., Weerheim, A., Kempenaar, J., Mulder, A., and Mommaas, A.M. Epidermal growth factor and temperature regulate keratinocyte differentiation. Arch Dermatol Res 289, 317, 1997.
32. Schmuth, M., Yosipovitch, G., Williams, M.L., Weber, F., Hintner, H., Ortiz-Urda, S., Rappersberger, K., Crumrine, D., Feingold, K.R., and Elias, P.M. Pathogenesis of the permeability barrier abnormality in epidermolytic hyperkeratosis. J Invest Dermatol 117, 837, 2001.
33. Park, K., Elias, P.M., Oda, Y., Mackenzie, D., Mauro, T., Holleran, W.M., and Uchida, Y. Regulation of cathelicidin antimicrobial peptide expression by an endoplasmic reticulum (ER) stress signaling, vitamin D receptor-independent pathway. J Biol Chem 286, 34121, 2011.
34. Celli, A., Sanchez, S., Behne, M., Hazlett, T., Gratton, E., and Mauro, T. The epidermal Ca(2 +) gradient: Measurement using the phasor representation of fluorescent lifetime imaging. Biophys J 98, 911, 2010.
35. Firooz, A., Sadr, B., Babakoohi, S., Sarraf-Yazdy, M., Fanian, F., Kazerouni-Timsar, A., Nassiri-Kashani, M., Naghizadeh, M.M., and Dowlati, Y. Variation of biophysical parameters of the skin with age, gender, and body region. ScientificWorldJournal 2012, 386936, 2012.
36. Kiatsurayanon, C., Niyonsaba, F., Smithrithee, R., Akiyama, T., Ushio, H., Hara, M., Okumura, K., Ikeda, S., and Ogawa, H. Host defense (antimicrobial) peptide, human beta-defensin-3, improves the function of the epithelial tight junction barrier in human keratinocytes. J Invest Dermatol 2014. DOI: 10.1038/jid.2014.143.
37. Skerrow, C.J., Clelland, D.G., and Skerrow, D. Changes to desmosomal antigens and lectin-binding sites during differentiation in normal human epidermis: a quantitative ultrastructural study. J Cell Sci 92(Pt 4), 667, 1989.
38. Gunathilake, R., Schurer, N.Y., Shoo, B.A., Celli, A., Hachem, J.P., Crumrine, D., Sirimanna, G., Feingold, K.R., Mauro, T.M., and Elias, P.M. pH-regulated mechanisms account for pigment-type differences in epidermal barrier function. J Invest Dermatol 129, 1719, 2009.
39. Matsumoto, M., Zhou, Y., Matsuo, S., Nakanishi, H., Hirose, K., Oura, H., Arase, S., Ishida-Yamamoto, A., Bando, Y., Izumi, K., Kiyonari, H., Oshima, N., Nakayama, R., Matsushima, A., Hirota, F., Mouri, Y., Kuroda, N., Sano, S., and Chaplin, D.D. Targeted deletion of the murine corneodesmosin gene delineates its essential role in skin and hair physiology. Proc Natl Acad Sci USA 105, 6720, 2008.
40. Vicanova, J., Mommaas, A.M., Mulder, A.A., Koerten, H.K., and Ponec, M. Impaired desquamation in the in vitro reconstructed human epidermis. Cell Tissue Res 286, 115, 1996.
41. 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.
42. Ghadially, R., Brown, B.E., Sequeira-Martin, S.M., Feingold, K.R., and Elias, P.M. The aged epidermal permeability barrier. Structural, functional, and lipid biochemical abnormalities in humans and a senescent murine model. J Clin Invest 95, 2281, 1995.
43. Elias, P.M. Epilogue: fixing the barrier-theory and rational deployment. In: Elias, P.M., and Feingold, K.R., eds. Skin Barrier. New York, NY: Taylor & Francis Group, 2006, pp. 591-599.
44. Kawada, C., Hasegawa, T., Watanabe, M., and Nomura, Y. Dietary glucosylceramide enhances tight junction function in skin epidermis via induction of claudin-1. Biosci Biotechnol Biochem 77, 867, 2013.
45. Hamanaka, S., Hara, M., Nishio, H., Otsuka, F., Suzuki, A., and Uchida, Y. Human epidermal glucosylceramides are major precursors of stratum corneum ceramides. J Invest Dermatol 119, 416, 2002.
46. Feingold, K.R. Thematic review series: skin lipids. The role of epidermal lipids in cutaneous permeability barrier homeostasis. J Lipid Res 48, 2531, 2007.
47. Warskulat, U., Reinen, A., Grether-Beck, S., Krutmann, J., and Haussinger, D. The osmolyte strategy of normal human keratinocytes in maintaining cell homeostasis. J Invest Dermatol 123, 516, 2004.
48. Elias, P., Ahn, S., Brown, B., Crumrine, D., and Feingold, K.R. Origin of the epidermal calcium gradient: regulation by barrier status and role of active vs passive mechanisms. J Invest Dermatol 119, 1269, 2002.
49. Behne, M.J., Barry, N.P., Hanson, K.M., Aronchik, I., Clegg, R.W., Gratton, E., Feingold, K., Holleran, W.M., Elias, P.M., and Mauro, T.M. Neonatal development of the stratum corneum pH gradient: localization and mechanisms leading to emergence of optimal barrier function. J Invest Dermatol 120, 998, 2003.
50. Fluhr, J.W., Mao-Qiang, M., Brown, B.E., Hachem, J.P., Moskowitz, D.G., Demerjian, M., Haftek, M., Serre, G., Crumrine, D., Mauro, T.M., Elias, P.M., and Feingold, K.R. Functional consequences of a neutral pH in neonatal rat stratum corneum. J Invest Dermatol 123, 140, 2004.
51. Denda, M., Sato, J., Masuda, Y., Tsuchiya, T., Koyama, J., Kuramoto, M., Elias, P.M., and Feingold, K.R. Exposure to a dry environment enhances epidermal permeability barrier function. J Invest Dermatol 111, 858, 1998.
52. Takei, K., Denda, S., Kumamoto, J., and Denda, M. Low environmental humidity induces synthesis and release of cortisol in an epidermal organotypic culture system. Exp Dermatol 22, 662, 2013.
53. Thakoersing, V.S., Ponec, M., and Bouwstra, J.A. Generation of human skin equivalents under submerged conditions-mimicking the in utero environment. Tissue Eng Part A 16, 1433, 2010.