Natural corneal cell-based microenvironment as prerequisite for balanced 3D corneal epithelial morphogenesis: A promising animal experiment-abandoning tool in ophthalmology

Tissue Engineering - Part C: Methods

Volumn 20, Issue 4, 2014, Pages 297-307

  Schulz, Simon ^a   Beck, David ^a   Laird, Dougal ^a   Steinberg, Thorsten ^a   Tomakidi, Pascal ^a   Reinhard, Thomas ^a   Eberwein, Philipp ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; ENDOTHELIAL CELLS; FIBROBLASTS; GENE EXPRESSION; MORPHOLOGY; OPHTHALMOLOGY; THREE DIMENSIONAL; TISSUE; TOOLS;

COLLAGEN SCAFFOLDS; ENGINEERED TISSUES; EPITHELIAL MORPHOGENESIS; EPITHELIAL TISSUE; INDIRECT IMMUNOFLUORESCENCE; KERATINOCYTE DIFFERENTIATION; MECHANISTIC STUDIES; MINIMUM REQUIREMENTS;

SCAFFOLDS (BIOLOGY);

BREAST CANCER RESISTANCE PROTEIN; CYTOKERATIN 12; CYTOKERATIN 19; FILAGGRIN; INVOLUCRIN;

ARTICLE; AUTOREGULATION; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CELL STRUCTURE; CELL TRANSFORMATION; COCULTURE; CORNEA EPITHELIUM; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOLOCALIZATION; IN VITRO STUDY; KERATINOCYTE; MESSENGER RNA SYNTHESIS; MICROENVIRONMENT; MORPHOGENESIS; MUSCLE REGENERATION; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; RNA ISOLATION; UPREGULATION;

ANIMAL EXPERIMENTATION; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL MARKERS; CELLS, CULTURED; CELLULAR MICROENVIRONMENT; COCULTURE TECHNIQUES; EPITHELIUM, CORNEAL; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; HUMANS; INTERMEDIATE FILAMENT PROTEINS; KERATINOCYTES; KI-67 ANTIGEN; MORPHOGENESIS; NEOPLASM PROTEINS; OPHTHALMOLOGY; PROTEIN PRECURSORS; STAINING AND LABELING;

EID: 84897384516     PISSN: 19373384     EISSN: 19373392     Source Type: Journal    
DOI: 10.1089/ten.tec.2013.0195     Document Type: Article

References (47)

1. Pearson, R.M. In-vitro techniques: can they replace animal testing? Hum Reprod 1, 559, 1986.
2. Matthews, R.A. Medical progress depends on animal models-doesn't it? J R Soc Med 101, 95, 2008.
3. Dickson, M.A., Hahn, W.C., Ino, Y., Ronfard, V., Wu, J.Y., Weinberg, R.A., et al. Human keratinocytes that express hTERT and also bypass a p16(INK4a)-enforced mechanism that limits life span become immortal yet retain normal growth and differentiation characteristics. Mol Cell Biol 20, 1436, 2000.
4. Rivetti di Val Cervo, P., Lena, A.M., Nicoloso, M., Rossi, S., Mancini, M., Zhou, H., et al. p63-microRNA feedback in keratinocyte senescence. Proc Natl Acad Sci USA 109, 1133, 2012.
5. Fusenig, N.E., Limat, A., Stark, H.J., and Breitkreutz, D. Modulation of the differentiated phenotype of keratinocytes of the hair follicle and from epidermis. J Dermatol Sci 7 Suppl, S142, 1994.
6. Presland, R.B., and Dale, B.A. Epithelial structural proteins of the skin and oral cavity: function in health and disease. Crit Rev Oral Biol Med 11, 383, 2000.
7. Schlotzer-Schrehardt, U., and Kruse, F.E. Identification and characterization of limbal stem cells. Exp Eye Res 81, 247, 2005.
8. Koster, M.I., and Roop, D.R. Mechanisms regulating epithelial stratification. Annu Rev Cell Dev Biol 23, 93, 2007.
9. Bragulla, H.H., and Homberger, D.G. Structure and functions of keratin proteins in simple, stratified, keratinized and cornified epithelia. J Anat 214, 516, 2009.
10. Lee, S.K., Teng, Y., Wong, H.K., Ng, T.K., Huang, L., Lei, P., et al. MicroRNA-145 regulates human corneal epithelial differentiation. PLoS One 6, e21249, 2011.
11. Eberwein, P., Steinberg, T., Schulz, S., Zimmermann, D., Accardi, R., Beck, D., et al. Expression of keratinocyte biomarkers is governed by environmental biomechanics. Eur J Cell Biol 90, 1029, 2011.
12. Chapman, S., Liu, X., Meyers, C., Schlegel, R., and McBride, A.A. Human keratinocytes are efficiently immortalized by a Rho kinase inhibitor. J Clin Invest 120, 2619, 2010.
13. Offord, E.A., Sharif, N.A., Mace, K., Tromvoukis, Y., Spillare, E.A., Avanti, O., et al. Immortalized human corneal epithelial cells for ocular toxicity and inflammation studies. Invest Ophthal Vis Sci 40, 1091, 1999.
14. Schmedt, T., Chen, Y., Nguyen, T.T., Li, S., Bonanno, J.A., and Jurkunas, U.V. Telomerase immortalization of human corneal endothelial cells yields functional hexagonal monolayers. PLoS One 7, e51427, 2012.
15. 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.
16. Tomakidi, P., Breitkreutz, D., Fusenig, N.E., Zoller, J., Kohl, A., and Komposch, G. Establishment of oral mucosa phenotype in vitro in correlation to epithelial anchorage. Cell Tissue Res 292, 355, 1998.
17. Roesch-Ely, M., Steinberg, T., Bosch, F.X., Mussig, E., Whitaker, N., Wiest, T., et al. Organotypic co-cultures allow for immortalized human gingival keratinocytes to reconstitute a gingival epithelial phenotype in vitro. Differentiation 74, 622, 2006.
18. Orwin, E.J., and Hubel, A. In vitro culture characteristics of corneal epithelial, endothelial, and keratocyte cells in a native collagen matrix. Tissue Eng 6, 307, 2000.
19. Reichl, S., Bednarz, J., and Muller-Goymann, C.C. Human corneal equivalent as cell culture model for in vitro drug permeation studies. Br J Ophthalmol 88, 560, 2004.
20. Meyer, L., Bednarz, J., Müller-Goymann, C., and Reichl, S. Esteraseaktivitä t eines organotypischen humanen Kornea-Konstrukts (HCC) als In-vitro-Modell fü r Permeationsuntersuchungen. Der Ophthalmol 102, 971, 2005.
21. Papini, S., Rosellini, A., Nardi, M., Giannarini, C., and Revoltella, R.P. Selective growth and expansion of human corneal epithelial basal stem cells in a three-dimensionalorgan culture. Differentiation 73, 61, 2005.
22. Proulx, S., d'Arc Uwamaliya, J., Carrier, P., Deschambeault, A., Audet, C., Giasson, C.J., et al. Reconstruction of a human cornea by the self-assembly approach of tissue engineering using the three native cell types. Mol Vis 16, 2192, 2010.
23. Fusenig, N.E., and Boukamp, P. Multiple stages and genetic alterations in immortalization, malignant transformation, and tumor progression of human skin keratinocytes. Mol Carcinog 23, 144, 1998.
24. Toouli, C.D., Huschtscha, L.I., Neumann, A.A., Noble, J.R., Colgin, L.M., Hukku, B., et al. Comparison of human mammary epithelial cells immortalized by simian virus 40 T-Antigen or by the telomerase catalytic subunit. Oncogene 21, 128, 2002.
25. Commission, E. Directive 2010/63/EU of the European Parliament and of the council of 22 September 2010 and ofthe council of 22 September 2010 on the protection of animals used for scientific purposes. 2010. http://eur-lex.europa. eu/LexUriServ/LexUriServ.do?uri=OJ:L:2010:276:0033: 0079:en:PDF.
26. Guenoun, J.M., Baudouin, C., Rat, P., Pauly, A., Warnet, J.M., and Brignole-Baudouin, F. In vitro study of inflammatory potential and toxicity profile of latanoprost, travoprost, and bimatoprost in conjunctiva-derived epithelial cells. Invest Ophthalmol Vis Sci 46, 2444, 2005.
27. Choy, C.K., Cho, P., Boost, M.V., and Benzie, I.F. Do multipurpose solutions damage porcine corneal epithelial cells? Optom Vis Sci 86, E447, 2009.
28. Pear, W.S., Nolan, G.P., Scott, M.L., and Baltimore, D. Production of high-titer helper-free retroviruses by transient transfection. Proc Natl Acad Sci USA 90, 8392, 1993.
29. Livak, K.J., and Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402, 2001.
30. Ordonez, P., and Di Girolamo, N. Limbal epithelial stem cells: role of the niche microenvironment. Stem cells 30, 100, 2012.
31. Mussig, E., Steinberg, T., Kohl, A., Chamulitrat, W., Komposch, G., and Tomakidi, P. Discrimination of epithelium-like and fibroblast-like phenotypes derived from ethanol-treated immortalised human gingival keratinocytes in epithelial equivalents. Cell Tissue Res 332, 57, 2008.
32. Winter, S., Kohl, A., Huppertz, A., Herold-Mende, C., Wiest, T., Komposch, G., et al. Expression of mRNAs encoding for growth factors, ECM molecules, and MMP13 in monocultures and co-cultures of human periodontal ligament fibroblasts and alveolar bone cells. Cell Tissue Res 319, 467, 2005.
33. Fuchs, E., and Horsley, V. More than one way to skin. Genes Dev 22, 976, 2008.
34. Tong, L., Corrales, R.M., Chen, Z., Villarreal, A.L., De Paiva, C.S., Beuerman, R., et al. Expression and regulation of cornified envelope proteins in human corneal epithelium. Invest Ophthalmol Vis Sci 47, 1938, 2006.
35. Ding, X.W., Wu, J.H., and Jiang, C.P. ABCG2: a potential marker of stem cells and novel target in stem cell and cancer therapy. Life Sci 86, 631, 2010.
36. Nubile, M., Lanzini, M., Miri, A., Pocobelli, A., Calienno, R., Curcio, C., et al. In vivo confocal microscopy in diagnosis of limbal stem cell deficiency. Am J Ophthalmol 155, 220, 2013.
37. Cresta, F.B., and Alves, M.R. [Evaluation of the corneal epithelium kinetics using cell proliferation markers]. Arq Bras Oftalmol 70, 953, 2007.
38. West-Mays, J.A., and Dwivedi, D.J. The keratocyte: corneal stromal cell with variable repair phenotypes. Int J Biochem Cell Biol 38, 1625, 2006.
39. Lundberg, A.S., Randell, S.H., Stewart, S.A., Elenbaas, B., Hartwell, K.A., Brooks, M.W., et al. Immortalization and transformation of primary human airway epithelial cells by gene transfer. Oncogene 21, 4577, 2002.
40. Steinberg, M.L., and Defendi, V. Transformation and immortalization of human keratinocytes by SV40. J Invest Dermatol 81, 131s, 1983.
41. Smola, H., Thiekotter, G., and Fusenig, N.E. Mutual induction of growth factor gene expression by epidermal-dermal cell interaction. J Cell Biol 122, 417, 1993.
42. Maas-Szabowski, N., Stark, H.J., and Fusenig, N.E. Keratinocyte growth regulation in defined organotypic cultures through IL-1-induced keratinocyte growth factor expression in resting fibroblasts. J Invest Dermatol 114, 1075, 2000.
43. Maas-Szabowski, N., Szabowski, A., Stark, H.J., Andrecht, S., Kolbus, A., Schorpp-Kistner, M., et al. Organotypic cocultures with genetically modified mouse fibroblasts as a tool to dissect molecular mechanisms regulating keratinocyte growth and differentiation. J Invest Dermatol 116, 816, 2001.
44. Stark, H.J., Szabowski, A., Fusenig, N.E., and Maas-Szabowski, N. Organotypic cocultures as skin equivalents: a complex and sophisticated in vitro system. Biol Proc Online 6, 55, 2004.
45. Watt, F.M., Jordan, P.W., and O'Neill, C.H. Cell shape controls terminal differentiation of human epidermal keratinocytes. Proc Natl Acad Sci USA 85, 5576, 1988.
46. Doyle, M.J., Zhou, S., Tanaka, K.K., Pisconti, A., Farina, N.H., Sorrentino, B.P., et al. Abcg2 labels multiple cell types in skeletal muscle and participates in muscle regeneration. J Cell Biol 195, 147, 2011.
47. Maas-Szabowski, N., Starker, A., and Fusenig, N.E. Epidermal tissue regeneration and stromal interaction in HaCaT cells is initiated by TGF-alpha. J Cell Sci 116, 2937, 2003.