3D in vitro model of a functional epidermal permeability barrier from human embryonic stem cells and induced pluripotent stem cells

Stem Cell Reports

Volumn 2, Issue 5, 2014, Pages 675-689

  Petrova, Anastasia ^a,e   Celli, Anna ^b   Jacquet, Laureen ^a   Dafou, Dimitra ^c,f   Crumrine, Debra ^b   Hupe, Melanie ^b   Arno, Matthew ^a   Hobbs, Carl ^a   Cvoro, Aleksandra ^d   Karagiannis, Panagiotis ^a   Devito, Liani ^a   Sun, Richard ^b   Adame, Lillian C ^b   Vaughan, Robert ^a   McGrath, John A ^a   Mauro, Theodora M ^b   Ilic, Dusko ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c GUY S HOSPITAL   (United Kingdom)

^d HOUSTON METHODIST RESEARCH INSTITUTE   (United States)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

^f ARISTOTLE UNIVERSITY OF THESSALONIKI   (Greece)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTOME; CYTOKERATIN 14; KRT14 PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

ARTICLE; CELL DIFFERENTIATION; CELL FUNCTION; CELL POPULATION; CONTROLLED STUDY; CULTURE MEDIUM; EMBRYO; EMBRYONIC STEM CELL; EPIDERMIS; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN EPIDERMAL EQUIVALENT; HUMIDITY; IN VITRO STUDY; KERATINOCYTE; PERMEABILITY BARRIER; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; SKIN PERMEABILITY; BIOLOGICAL MODEL; CELL CULTURE; CULTURE TECHNIQUE; CYTOLOGY; DNA METHYLATION; EPITHELIAL MESENCHYMAL TRANSITION; GENETICS; METABOLISM; NUCLEAR REPROGRAMMING; PATHOLOGY; PERMEABILITY; PRINCIPAL COMPONENT ANALYSIS; TERATOMA; GENE EXPRESSION; SKIN; SKIN BIOPSY;

CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELLS, CULTURED; CELLULAR REPROGRAMMING; DNA METHYLATION; EMBRYONIC STEM CELLS; EPIDERMIS; EPITHELIAL-MESENCHYMAL TRANSITION; HUMANS; INDUCED PLURIPOTENT STEM CELLS; KERATIN-14; KERATINOCYTES; MODELS, BIOLOGICAL; PERMEABILITY; PRINCIPAL COMPONENT ANALYSIS; TERATOMA; TRANSCRIPTION FACTORS; TRANSCRIPTOME;

EID: 84900321798     PISSN: 22136711     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stemcr.2014.03.009     Document Type: Article

References (54)

1. D. Aberdam, K. Gambaro, P. Rostagno, E. Aberdam, S. de la Forest Divonne, and M. Rouleau Key role of p63 in BMP-4-induced epidermal commitment of embryonic stem cells Cell Cycle 6 2007 291 294
2. J. Agren, G. Sjörs, and G. Sedin Ambient humidity influences the rate of skin barrier maturation in extremely preterm infants J. Pediatr. 148 2006 613 617
3. M. Bellin, M.C. Marchetto, F.H. Gage, and C.L. Mummery Induced pluripotent stem cells: the new patient? Nat. Rev. Mol. Cell Biol. 13 2012 713 726
4. J.R. Bickenbach, and D.R. Roop Transduction of a preselected population of human epidermal stem cells: consequences for gene therapy Proc. Assoc. Am. Physicians 111 1999 184 189
5. C. Blanpain, and E. Fuchs p63: revving up epithelial stem-cell potential Nat. Cell Biol. 9 2007 731 733
6. C. Blanpain, and E. Fuchs Epidermal homeostasis: a balancing act of stem cells in the skin Nat. Rev. Mol. Cell Biol. 10 2009 207 217
7. 2+)-signaling properties in keratinocytes and in COS-1 cells overexpressing the secretory-pathway Ca(2+)-ATPase SPCA1 Cell Calcium 34 2003 157 162
8. a+-dependent keratinocyte adhesion and differentiation is mediated via the sphingolipid pathway: a therapeutic target for Darier's disease J. Invest. Dermatol. 132 2012 1188 1195
9. C. Chang, and A. Hemmati-Brivanlou Cell fate determination in embryonic ectoderm J. Neurobiol. 36 1998 128 151
10. X. Cheng, L. Ying, L. Lu, A.M. Galvão, J.A. Mills, H.C. Lin, D.N. Kotton, S.S. Shen, M.C. Nostro, and J.K. Choi et al. Self-renewing endodermal progenitor lines generated from human pluripotent stem cells Cell Stem Cell 10 2012 371 384
11. C.P. Crum, and F.D. McKeon p63 in epithelial survival, germ cell surveillance, and neoplasia Annu. Rev. Pathol. 5 2010 349 371
12. M. Del Rio, F. Larcher, F. Serrano, A. Meana, M. Muñoz, M. Garcia, E. Muñoz, C. Martin, A. Bernad, and J.L. Jorcano A preclinical model for the analysis of genetically modified human skin in vivo Hum. Gene Ther. 13 2002 959 968
13. M. Denda, J. Sato, Y. Masuda, T. Tsuchiya, J. Koyama, M. Kuramoto, P.M. Elias, and K.R. Feingold Exposure to a dry environment enhances epidermal permeability barrier function J. Invest. Dermatol. 111 1998 858 863
14. P.M. Elias Epidermal lipids, barrier function, and desquamation J. Invest. Dermatol. 80 Suppl 1983 44s 49s
15. P.M. Elias Structure and function of the stratum corneum extracellular matrix J. Invest. Dermatol. 132 2012 2131 2133
16. P.M. Elias, S.K. Ahn, M. Denda, B.E. Brown, D. Crumrine, L.K. Kimutai, L. Kömüves, S.H. Lee, and K.R. Feingold Modulations in epidermal calcium regulate the expression of differentiation-specific markers J. Invest. Dermatol. 119 2002 1128 1136
17. C. Götz, R. Pfeiffer, J. Tigges, V. Blatz, C. Jäckh, E.M. Freytag, E. Fabian, R. Landsiedel, H.F. Merk, and J. Krutmann et al. Xenobiotic metabolism capacities of human skin in comparison with a 3D epidermis model and keratinocyte-based cell culture as in vitro alternatives for chemical testing: activating enzymes (Phase I) Exp. Dermatol. 21 2012 358 363
18. M. Gschwandtner, M. Mildner, V. Mlitz, F. Gruber, L. Eckhart, T. Werfel, R. Gutzmer, P.M. Elias, and E. Tschachler Histamine suppresses epidermal keratinocyte differentiation and impairs skin barrier function in a human skin model Allergy 68 2013 37 47
19. K. Hanley, Y. Jiang, P.M. Elias, K.R. Feingold, and M.L. Williams Acceleration of barrier ontogenesis in vitro through air exposure Pediatr. Res. 41 1997 293 299
20. D.C. Hay, D. Zhao, J. Fletcher, Z.A. Hewitt, D. McLean, A. Urruticoechea-Uriguen, J.R. Black, C. Elcombe, J.A. Ross, R. Wolf, and W. Cui Efficient differentiation of hepatocytes from human embryonic stem cells exhibiting markers recapitulating liver development in vivo Stem Cells 26 2008 894 902
21. + exchanger 1 plasma membrane localization Am. J. Pathol. 170 2007 2055 2067
22. D. Ilic, E. Stephenson, V. Wood, L. Jacquet, D. Stevenson, A. Petrova, N. Kadeva, S. Codognotto, H. Patel, and M. Semple et al. Derivation and feeder-free propagation of human embryonic stem cells under xeno-free conditions Cytotherapy 14 2012 122 128
23. M. Itoh, N. Umegaki-Arao, Z. Guo, L. Liu, C.A. Higgins, and A.M. Christiano Generation of 3D skin equivalents fully reconstituted from human induced pluripotent stem cells (iPSCs) PLoS ONE 8 2013 e77673
24. L. Jacquet, E. Stephenson, R. Collins, H. Patel, J. Trussler, R. Al-Bedaery, P. Renwick, C. Ogilvie, R. Vaughan, and D. Ilic Strategy for the creation of clinical grade hESC line banks that HLA-match a target population EMBO Mol Med 5 2013 10 17
25. A.E. Kalinin, A.V. Kajava, and P.M. Steinert Epithelial barrier function: assembly and structural features of the cornified cell envelope Bioessays 24 2002 789 800
26. C. Katagiri, J. Sato, J. Nomura, and M. Denda Changes in environmental humidity affect the water-holding property of the stratum corneum and its free amino acid content, and the expression of filaggrin in the epidermis of hairless mice J. Dermatol. Sci. 31 2003 29 35
27. L.G. Kömüves, K. Hanley, Y. Jiang, C. Katagiri, P.M. Elias, M.L. Williams, and K.R. Feingold Induction of selected lipid metabolic enzymes and differentiation-linked structural proteins by air exposure in fetal rat skin explants J. Invest. Dermatol. 112 1999 303 309
28. S. Küchler, K. Strüver, and W. Friess Reconstructed skin models as emerging tools for drug absorption studies Expert Opin. Drug Metab. Toxicol. 9 2013 1255 1263
29. N. Linde, C.M. Gutschalk, C. Hoffmann, D. Yilmaz, and M.M. Mueller Integrating macrophages into organotypic co-cultures: a 3D in vitro model to study tumor-associated macrophages PLoS ONE 7 2012 e40058
30. A. Medawar, T. Virolle, P. Rostagno, S. de la Forest-Divonne, K. Gambaro, M. Rouleau, and D. Aberdam DeltaNp63 is essential for epidermal commitment of embryonic stem cells PLoS ONE 3 2008 e3441
31. M. Mildner, J. Jin, L. Eckhart, S. Kezic, F. Gruber, C. Barresi, C. Stremnitzer, M. Buchberger, V. Mlitz, and C. Ballaun et al. Knockdown of filaggrin impairs diffusion barrier function and increases UV sensitivity in a human skin model J. Invest. Dermatol. 130 2010 2286 2294
32. J.C. Murray, G. Stingl, H.K. Kleinman, G.R. Martin, and S.I. Katz Epidermal cells adhere preferentially to type IV (basement membrane) collagen J. Cell Biol. 80 1979 197 202
33. Z. Nemes, and P.M. Steinert Bricks and mortar of the epidermal barrier Exp. Mol. Med. 31 1999 5 19
34. X. Nissan, L. Larribere, M. Saidani, I. Hurbain, C. Delevoye, J. Feteira, G. Lemaitre, M. Peschanski, and C. Baldeschi Functional melanocytes derived from human pluripotent stem cells engraft into pluristratified epidermis Proc. Natl. Acad. Sci. USA 108 2011 14861 14866
35. A.E. Palmer, and R.Y. Tsien Measuring calcium signaling using genetically targetable fluorescent indicators Nat. Protoc. 1 2006 1057 1065
36. M. Ponec, S. Gibbs, G. Pilgram, E. Boelsma, H. Koerten, J. Bouwstra, and M. Mommaas Barrier function in reconstructed epidermis and its resemblance to native human skin Skin Pharmacol. Appl. Skin Physiol. 14 Suppl 1 2001 63 71
37. S. Pozzi, F. Zambelli, D. Merico, G. Pavesi, A. Robert, P. Maltère, X. Gidrol, R. Mantovani, and M.A. Vigano Transcriptional network of p63 in human keratinocytes PLoS ONE 4 2009 e5008
38. G. Richard Molecular genetics of the ichthyoses Am. J. Med. Genet. C. Semin. Med. Genet. 131C 2004 32 44
39. D.A. Robinton, and G.Q. Daley The promise of induced pluripotent stem cells in research and therapy Nature 481 2012 295 305
40. J. Sato, M. Denda, S. Chang, P.M. Elias, and K.R. Feingold Abrupt decreases in environmental humidity induce abnormalities in permeability barrier homeostasis J. Invest. Dermatol. 119 2002 900 904
41. J. Segre Complex redundancy to build a simple epidermal permeability barrier Curr. Opin. Cell Biol. 15 2003 776 782
42. J.A. Segre Epidermal barrier formation and recovery in skin disorders J. Clin. Invest. 116 2006 1150 1158
43. C.L. Simpson, S. Kojima, and S. Getsios RNA interference in keratinocytes and an organotypic model of human epidermis Methods Mol. Biol. 585 2010 127 146
44. C.L. Simpson, D.M. Patel, and K.J. Green Deconstructing the skin: cytoarchitectural determinants of epidermal morphogenesis Nat. Rev. Mol. Cell Biol. 12 2011 565 580
45. F.J. Smith, A.D. Irvine, A. Terron-Kwiatkowski, A. Sandilands, L.E. Campbell, Y. Zhao, H. Liao, A.T. Evans, D.R. Goudie, and S. Lewis-Jones et al. Loss-of-function mutations in the gene encoding filaggrin cause ichthyosis vulgaris Nat. Genet. 38 2006 337 342
46. E. Stephenson, L. Jacquet, C. Miere, V. Wood, N. Kadeva, G. Cornwell, S. Codognotto, Y. Dajani, P. Braude, and D. Ilic Derivation and propagation of human embryonic stem cell lines from frozen embryos in an animal product-free environment Nat. Protoc. 7 2012 1366 1381
47. C.D. Stern Neural induction: old problem, new findings, yet more questions Development 132 2005 2007 2021
48. K. Takei, S. Denda, J. Kumamoto, and M. Denda Low environmental humidity induces synthesis and release of cortisol in an epidermal organotypic culture system Exp. Dermatol. 22 2013 662 664
49. V.S. Thakoersing, M. Ponec, and J.A. Bouwstra Generation of human skin equivalents under submerged conditions-mimicking the in utero environment Tissue Eng. Part A 16 2010 1433 1441
50. V.S. Thakoersing, G.S. Gooris, A. Mulder, M. Rietveld, A. El Ghalbzouri, and J.A. Bouwstra Unraveling barrier properties of three different in-house human skin equivalents Tissue Eng. Part C Methods 18 2012 1 11
51. C.-L. Tu, D.A. Crumrine, M.-Q. Man, W. Chang, H. Elalieh, M. You, P.M. Elias, and D.D. Bikle Ablation of the calcium-sensing receptor in keratinocytes impairs epidermal differentiation and barrier function J. Invest. Dermatol. 132 2012 2350 2359
52. H. Vanbokhoven, G. Melino, E. Candi, and W. Declercq p63, a story of mice and men J. Invest. Dermatol. 131 2011 1196 1207
53. L. Warren, P.D. Manos, T. Ahfeldt, Y.H. Loh, H. Li, F. Lau, W. Ebina, P.K. Mandal, Z.D. Smith, and A. Meissner et al. Highly efficient reprogramming to pluripotency and directed differentiation of human cells with synthetic modified mRNA Cell Stem Cell 7 2010 618 630
54. E. Yakubov, G. Rechavi, S. Rozenblatt, and D. Givol Reprogramming of human fibroblasts to pluripotent stem cells using mRNA of four transcription factors Biochem. Biophys. Res. Commun. 394 2010 189 193