Substrate elasticity as biomechanical modulator of tissue homeostatic parameters in corneal keratinocytes

Experimental Cell Research

Volumn 319, Issue 12, 2013, Pages 1889-1901

  Moers, Katharina ^a   Steinberg, Thorsten ^a   Schlunck, Günther ^a   Reinhard, Thomas ^a   Tomakidi, Pascal ^a   Eberwein, Philipp ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Biomechanics; Cornea; Differentiation; Elasticity; Proliferation; Tissue homeostasis

Indexed keywords

ACTIN; BETA1 INTEGRIN; BIOLOGICAL MARKER; BREAST CANCER RESISTANCE PROTEIN; CYTOKERATIN 12; CYTOKERATIN 19; FILLAGRIN; FOCAL ADHESION KINASE 1; INVOLUCRIN; MESSENGER RNA; NANOMATERIAL; UNCLASSIFIED DRUG;

ARTICLE; BIOMECHANICS; CELL DIFFERENTIATION; CELL FUNCTION; CELL PROLIFERATION; CORNEA; ELASTICITY; GENE EXPRESSION; HOMEOSTASIS; HUMAN; HUMAN CELL; KERATINOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION;

EID: 84879605280     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2013.05.002     Document Type: Article

References (46)

1. Discher D.E., Janmey P., Wang Y.L. Tissue cells feel and respond to the stiffness of their substrate. Science 2005, 310:1139-1143.
2. Kim D.J., Lee J.M., Park J.G., Chung B.G. A self-assembled monolayer-based micropatterned array for controlling cell adhesion and protein adsorption. Biotechnol. Bioeng. 2011, 108:1194-1202.
3. Wang Y.C., Ho C.C. Micropatterning of proteins and mammalian cells on biomaterials. FASEB J. 2004, 18:525-527.
4. Wang Y., Wang G., Luo X., Qiu J., Tang C. Substrate stiffness regulates the proliferation, migration, and differentiation of epidermal cells. Burns 2012, 38:414-420.
5. Pizzo A.M., Kokini K., Vaughn L.C., Waisner B.Z., Voytik-Harbin S.L. Extracellular matrix (ECM) microstructural composition regulates local cell-ECM biomechanics and fundamental fibroblast behavior: a multidimensional perspective. J. Appl. Physiol. 2005, 98:1909-1921.
6. Titushkin I.A., Shin J., Cho M. A new perspective for stem-cell mechanobiology: biomechanical control of stem-cell behavior and fate. Crit. Rev. Biomed. Eng. 2010, 38:393-433.
7. Last J.A., Thomasy S.M., Croasdale C.R., Russell P., Murphy C.J. Compliance profile of the human cornea as measured by atomic force microscopy. Micron 2012, 43:1293-1298.
8. Zhang M., Zheng Y.P., Mak A.F. Estimating the effective Young's modulus of soft tissues from indentation tests-nonlinear finite element analysis of effects of friction and large deformation. Med. Eng. Phys. 1997, 19:512-517.
9. Scholzen T., Gerdes J. The Ki-67 protein: from the known and the unknown. J. Cell. Physiol. 2000, 182:311-322.
10. Eberwein P., Steinberg T., Schulz S., Zimmermann D., Accardi R., Beck D., Reinhard T., Tomakidi P. Expression of keratinocyte biomarkers is governed by environmental biomechanics. Eur. J. Cell Biol. 2011, 90:1029-1040.
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. Schlotzer-Schrehardt U., Kruse F.E. Identification and characterization of limbal stem cells. Exp. Eye Res. 2005, 81:247-264.
13. 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.
14. 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.
15. Z. Erdei, B. Sarkadi, A. Brozik, K. Szebenyi, G. Varady, V. Mako, A. Pentek, T.I. Orban and A. Apati, Dynamic ABCG2 expression in human embryonic stem cells provides the basis for stress response, Eur. Biophys. J. 42(2-3): (2013) 169-79. doi: 10.1007/s00249-012-0838-0 (Epub 2012 Aug 1).
16. O'Connor R.S., Hao X., Shen K., Bashour K., Akimova T., Hancock W.W., Kam L.C., Milone M.C. Substrate rigidity regulates human T cell activation and proliferation. J Immunol. 2012, 189:1330-1339.
17. Watt F.M. Role of integrins in regulating epidermal adhesion, growth and differentiation. EMBO J. 2002, 21:3919-3926.
18. Parsons J.T. Focal adhesion kinase: the first ten years. J. Cell Sci. 2003, 116:1409-1416.
19. Mitra S.K., Hanson D.A., Schlaepfer D.D. Focal adhesion kinase: in command and control of cell motility. Nat. Rev. Mol. Cell Biol. 2005, 6:56-68.
20. Hamadi A., Deramaudt T.B., Takeda K., Ronde P. Hyperphosphorylated FAK delocalizes from focal adhesions to membrane ruffles. J. Oncol. 2010.
21. Webb D.J., Donais K., Whitmore L.A., Thomas S.M., Turner C.E., Parsons J.T., Horwitz A.F. FAK-Src signalling through paxillin, ERK and MLCK regulates adhesion disassembly. Nat. Cell Biol. 2004, 6:154-161.
22. Tocce E.J., Smirnov V.K., Kibalov D.S., Liliensiek S.J., Murphy C.J., Nealey P.F. The ability of corneal epithelial cells to recognize high aspect ratio nanostructures. Biomaterials 2010, 31:4064-4072.
23. 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.
24. Schlunck G., Han H., Wecker T., Kampik D., Meyer-ter-Vehn T., Grehn F. Substrate rigidity modulates cell matrix interactions and protein expression in human trabecular meshwork cells. Invest. Ophthalmol. Vis. Sci. 2008, 49:262-269.
25. Pear W.S., Nolan G.P., Scott M.L., Baltimore D. Production of high-titer helper-free retroviruses by transient transfection. Proc. Nat. Acad. Sci. USA 1993, 90:8392-8396.
26. 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.
27. de Rooij J., Kerstens A., Danuser G., Schwartz M.A., Waterman-Storer C.M. Integrin-dependent actomyosin contraction regulates epithelial cell scattering. J. Cell Biol. 2005, 171:153-164.
28. Pelham R.J., Wang Y. Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc. Nat. Acad. Sci. USA 1997, 94:13661-13665.
29. 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.
30. Ziegler N., Alonso A., Steinberg T., Woodnutt D., Kohl A., Mussig E., Schulz S., Tomakidi P. Mechano-transduction in periodontal ligament cells identifies activated states of MAP-kinases p42/44 and p38-stress kinase as a mechanism for MMP-13 expression. BMC Cell Biol. 2010, 11:10.
31. Lu L., Reinach P.S., Kao W.W. Corneal epithelial wound healing. Exp. Biol. Med. (Maywood) 2001, 226:653-664.
32. Lehrer M.S., Sun T.T., Lavker R.M. Strategies of epithelial repair: modulation of stem cell and transit amplifying cell proliferation. J. Cell Sci. 1998, 111(Pt 19):2867-2875.
33. Sudha B., Sitalakshmi G., Iyer G.K., Krishnakumar S. Putative stem cell markers in limbal epithelial cells cultured on intact and denuded human amniotic membrane. Indian J. Med. Res. 2008, 128:149-156.
34. Joseph A., Powell-Richards A.O., Shanmuganathan V.A., Dua H.S. Epithelial cell characteristics of cultured human limbal explants. Br. J. Ophthalmol. 2004, 88:393-398.
35. Poli M., Janin H., Justin V., Auxenfans C., Burillon C., Damour O. Keratin 13 immunostaining in corneal impression cytology for the diagnosis of limbal stem cell deficiency. Invest. Ophthalmol. Vis. Sci. 2011, 52:9411-9415.
36. 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.
37. Chen C.S., Tan J., Tien J. Mechanotransduction at cell-matrix and cell-cell contacts. Annu. Rev. Biomed. Eng. 2004, 6:275-302.
38. Wozniak M.A., Modzelewska K., Kwong L., Keely P.J. Focal adhesion regulation of cell behavior. Biochim. Biophys. Acta 2004, 1692:103-119.
39. Oakes P.W., Beckham Y., Stricker J., Gardel M.L. Tension is required but not sufficient for focal adhesion maturation without a stress fiber template. J. Cell Biol. 2012, 196:363-374.
40. Meller D., Pires R.T., Tseng S.C. Ex vivo preservation and expansion of human limbal epithelial stem cells on amniotic membrane cultures. Br. J. Ophthalmol. 2002, 86:463-471.
41. Rama P., Bonini S., Lambiase A., Golisano O., Paterna P., De Luca M., Pellegrini G. Autologous fibrin-cultured limbal stem cells permanently restore the corneal surface of patients with total limbal stem cell deficiency. Transplantation 2001, 72:1478-1485.
42. Rama P., Matuska S., Paganoni G., Spinelli A., De Luca M., Pellegrini G. Limbal stem-cell therapy and long-term corneal regeneration. N. Engl. J. Med. 2010, 363:147-155.
43. Dean M., Rzhetsky A., Allikmets R. The human ATP-binding cassette (ABC) transporter superfamily. Genome Res. 2001, 11:1156-1166.
44. Basseville A., Tamaki A., Ierano C., Trostel S., Ward Y., Robey R.W., Hegde R.S., Bates S.E. Histone deacetylase inhibitors influence chemotherapy transport by modulating expression and trafficking of a common polymorphic variant of the ABCG2 efflux transporter. Cancer Res. 2012, 72:3642-3651.
45. Pankow S., Bamberger C., Klippel A., Werner S. Regulation of epidermal homeostasis and repair by phosphoinositide 3-kinase. J. Cell Sci. 2006, 119:4033-4046.
46. Woods M., Pant R., Mallya S.M. Cyclin D1 and cyclin D-dependent kinases enhance oral keratinocyte proliferation but do not block keratinocyte differentiation. Int. J. Oncol. 2010, 37:1471-1475.