Expression of keratinocyte biomarkers is governed by environmental biomechanics

European Journal of Cell Biology

Volumn 90, Issue 12, 2011, Pages 1029-1040

  Eberwein, Philipp ^a   Steinberg, Thorsten ^a   Schulz, Simon ^a   Zimmermann, Dominik ^b   Accardi, Rosita ^c   Beck, David ^a   Reinhard, Thomas ^a   Tomakidi, Pascal ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c INTERNATIONAL AGENCY FOR RESEARCH ON CANCER   (France)

Author keywords

Biomechanics; Cornea; Immortalization; Keratinocytes; Pillars

Indexed keywords

CYTOKERATIN 12; FILAGGRIN; INVOLUCRIN;

ARTICLE; BIOMECHANICS; CELL ADHESION; CELL DIFFERENTIATION; CELL IMMORTALIZATION; CELL PROLIFERATION; CONTROLLED STUDY; CORNEA; EPITHELIUM CELL; HUMAN; HUMAN CELL; KERATINOCYTE; MORPHOGENESIS; PRIORITY JOURNAL; PROPENSITY SCORE; PROTEIN EXPRESSION; STEM CELL;

BIOLOGICAL MARKERS; BIOMECHANICS; CELL DIFFERENTIATION; CELLS, CULTURED; CORNEA; HUMANS; KERATINOCYTES;

EID: 80054857287     PISSN: 01719335     EISSN: 16181298     Source Type: Journal    
DOI: 10.1016/j.ejcb.2011.08.005     Document Type: Article

References (41)

1. Adhikary G., Crish J., Lass J., Eckert R.L. Regulation of involucrin expression in normal human corneal epithelial cells: a role for activator protein one. Invest. Ophthalmol. Vis. Sci. 2004, 45:1080-1087.
2. Alenghat F.J., Ingber D.E. Mechanotransduction: all signals point to cytoskeleton, matrix, and integrins. Sci. STKE 2002, 2002:pe6.
3. Araki-Sasaki K., Ohashi Y., Sasabe T., Hayashi K., Watanabe H., Tano Y., Handa H. An SV40-immortalized human corneal epithelial cell line and its characterization. Invest. Ophthalmol. Vis. Sci. 1995, 36:614-621.
4. Bryan T.M., Reddel R.R. SV40-induced immortalization of human cells. Crit. Rev. Oncog. 1994, 5:331-357.
5. Budak M.T., Alpdogan O.S., Zhou M., Lavker R.M., Akinci M.A., Wolosin J.M. Ocular surface epithelia contain ABCG2-dependent side population cells exhibiting features associated with stem cells. J. Cell Sci. 2005, 118:1715-1724.
6. Castro-Munozledo F. Development of a spontaneous permanent cell line of rabbit corneal epithelial cells that undergoes sequential stages of differentiation in cell culture. J. Cell Sci. 1994, 107(Pt 8):2343-2351.
7. Chen H., Yan Y., Davidson T.L., Shinkai Y., Costa M. Hypoxic stress induces dimethylated histone H3 lysine 9 through histone methyltransferase G9a in mammalian cells. Cancer Res. 2006, 66:9009-9016.
8. D'Sa D.J., de Juan Pardo E.M., de las Rivas Astiz R., Sen S., Kumar S. High-throughput indentational elasticity measurements of hydrogel extracellular matrix substrates. Appl. Phys. Lett. 2009, 95:63701-63703.
9. Discher D.E., Janmey P., Wang Y.L. Tissue cells feel and respond to the stiffness of their substrate. Science 2005, 310:1139-1143.
10. Doi Y., Mizuno T., Maki Y., Jin S., Mizoguchi H., Ikeyama M., Doi M., Michikawa M., Takeuchi H., Suzumura A. Microglia activated with the toll-like receptor 9 ligand CpG attenuate oligomeric amyloid {beta} neurotoxicity in in vitro and in vivo models of Alzheimer's disease. Am. J. Pathol. 2009, 175:2121-2132.
11. Espana E.M., Di Pascuale M.A., He H., Kawakita T., Raju V.K., Liu C.Y., Tseng S.C. Characterization of corneal pannus removed from patients with total limbal stem cell deficiency. Invest. Ophthalmol. Vis. Sci. 2004, 45:2961-2966.
12. Furukawa T., Duguid W.P., Rosenberg L., Viallet J., Galloway D.A., Tsao M.S. Long-term culture and immortalization of epithelial cells from normal adult human pancreatic ducts transfected by the E6E7 gene of human papilloma virus 16. Am. J. Pathol. 1996, 148:1763-1770.
13. Gipson I.K., Spurr-Michaud S., Argueso P., Tisdale A., Ng T.F., Russo C.L. Mucin gene expression in immortalized human corneal-limbal and conjunctival epithelial cell lines. Invest. Ophthalmol. Vis. Sci. 2003, 44:2496-2506.
14. Ingber D.E. Mechanobiology and diseases of mechanotransduction. Ann. Med. 2003, 35:564-577.
15. Jaalouk D.E., Lammerding J. Mechanotransduction gone awry. Nat. Rev. Mol. Cell Biol. 2009, 10:63-73.
16. Kalinin A.E., Kajava A.V., Steinert P.M. Epithelial barrier function: assembly and structural features of the cornified cell envelope. Bioessays 2002, 24:789-800.
17. Koh W.G., Itle L.J., Pishko M.V. Molding of hydrogel microstructures to create multiphenotype cell microarrays. Anal. Chem. 2003, 75:5783-5789.
18. Krishnamurthy P., Ross D.D., Nakanishi T., Bailey-Dell K., Zhou S., Mercer K.E., Sarkadi B., Sorrentino B.P., Schuetz J.D. The stem cell marker Bcrp/ABCG2 enhances hypoxic cell survival through interactions with heme. J. Biol. Chem. 2004, 279:24218-24225.
19. Kubo E., Fatma N., Sharma P., Shinohara T., Chylack L.T., Akagi Y., Singh D.P. Transactivation of involucrin, a marker of differentiation in keratinocytes, by lens epithelium-derived growth factor (LEDGF). J. Mol. Biol. 2002, 320:1053-1063.
20. Lambert A., Ekambaram M., Robinson N., Eckert R.L. Transglutaminase reactivity of human involucrin. Skin Pharmacol. Appl. Skin Physiol. 2000, 13:17-30.
21. Li G., Fridman R., Kim H.R. Tissue inhibitor of metalloproteinase-1 inhibits apoptosis of human breast epithelial cells. Cancer Res. 1999, 59:6267-6275.
22. Li W., Chen Y.T., Hayashida Y., Blanco G., Kheirkah A., He H., Chen S.Y., Liu C.Y., Tseng S.C. Down-regulation of Pax6 is associated with abnormal differentiation of corneal epithelial cells in severe ocular surface diseases. J. Pathol. 2008, 214:114-122.
23. Liu C.Y., Zhu G., Westerhausen-Larson A., Converse R., Kao C.W., Sun T.T., Kao W.W. Cornea-specific expression of K12 keratin during mouse development. Curr. Eye Res. 1993, 12:963-974.
24. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 2001, 25:402-408.
25. Mohan R.R., Possin D.E., Sinha S., Wilson S.E. Development of genetically engineered tet HPV16-E6/E7 transduced human corneal epithelial clones having tight regulation of proliferation and normal differentiation. Exp. Eye Res. 2003, 77:395-407.
26. Mussig E., Schulz S., Spatz J.P., Ziegler N., Tomakidi P., Steinberg T. Soft micropillar interfaces of distinct biomechanics govern behaviour of periodontal cells. Eur. J. Cell Biol. 2010, 89:315-325.
27. Nicolas A., Safran S.A. Limitation of cell adhesion by the elasticity of the extracellular matrix. Biophys. J. 2006, 91:61-73.
28. Papini S., Rosellini A., Nardi M., Giannarini C., Revoltella R.P. Selective growth and expansion of human corneal epithelial basal stem cells in a three-dimensional-organ culture. Differentiation 2005, 73:61-68.
29. Pear W.S., Nolan G.P., Scott M.L., Baltimore D. Production of high-titer helper-free retroviruses by transient transfection. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:8392-8396.
30. Ray J.M., Stetler-Stevenson W.G. Gelatinase A activity directly modulates melanoma cell adhesion and spreading. EMBO J. 1995, 14:908-917.
31. Rice J.C., Allis C.D. Histone methylation versus histone acetylation: new insights into epigenetic regulation. Curr. Opin. Cell Biol. 2001, 13:263-273.
32. Roesch-Ely M., Steinberg T., Bosch F.X., Mussig E., Whitaker N., Wiest T., Kohl A., Komposch G., Tomakidi P. Organotypic co-cultures allow for immortalized human gingival keratinocytes to reconstitute a gingival epithelial phenotype in vitro. Differentiation 2006, 74:622-637.
33. Schlotzer-Schrehardt U., Kruse F.E. Identification and characterization of limbal stem cells. Exp. Eye Res. 2005, 81:247-264.
34. Slack J.M. Stem cells in epithelial tissues. Science 2000, 287:1431-1433.
35. Smith F.J., Irvine A.D., Terron-Kwiatkowski A., Sandilands A., Campbell L.E., Zhao Y., Liao H., Evans A.T., Goudie D.R., Lewis-Jones S., Arseculeratne G., Munro C.S., Sergeant A., O'Regan G., Bale S.J., Compton J.G., DiGiovanna J.J., Presland R.B., Fleckman P., McLean W.H. Loss-of-function mutations in the gene encoding filaggrin cause ichthyosis vulgaris. Nat. Genet. 2006, 38:337-342.
36. Soltaninia J., Boulton M., Armitage W.J., Albon J. Regulation of corneal epithelial homeostasis in transplantable corneas. Invest. Ophthalmol. Vis. Sci. 2004, 45:1460.
37. Stark H.J., Boehnke K., Mirancea N., Willhauck M.J., Pavesio A., Fusenig N.E., Boukamp P. Epidermal homeostasis in long-term scaffold-enforced skin equivalents. J. Invest. Dermatol. Symp. Proc. 2006, 11:93-105.
38. Steinberg T., Schulz S., Spatz J.P., Grabe N., Mussig E., Kohl A., Komposch G., Tomakidi P. Early keratinocyte differentiation on micropillar interfaces. Nano Lett. 2007, 7:287-294.
39. Steinert P.M., Marekov L.N. The proteins elafin, filaggrin, keratin intermediate filaments, loricrin, and small proline-rich proteins 1 and 2 are isodipeptide cross-linked components of the human epidermal cornified cell envelope. J. Biol. Chem. 1995, 270:17702-17711.
40. Tong L., Corrales R.M., Chen Z., Villarreal A.L., De Paiva C.S., Beuerman R., Li D.Q., Pflugfelder S.C. Expression and regulation of cornified envelope proteins in human corneal epithelium. Invest. Ophthalmol. Vis. Sci. 2006, 47:1938-1946.
41. Zhou S., Schuetz J.D., Bunting K.D., Colapietro A.M., Sampath J., Morris J.J., Lagutina I., Grosveld G.C., Osawa M., Nakauchi H., Sorrentino B.P. The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype. Nat. Med. 2001, 7:1028-1034.