Influence of extracellular matrix proteins and substratum topography on corneal epithelial cell alignment and migration

Tissue Engineering - Part A

Volumn 19, Issue 15-16, 2013, Pages 1713-1722

  Raghunathan, Vijaykrishna ^a   McKee, Clayton ^a   Cheung, Wai ^a   Naik, Rachel ^a   Nealey, Paul F ^b   Russell, Paul ^a   Murphy, Christopher J ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b University of Wisconsin Madison   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMIMETICS; BIOPHYSICS; CELLS; COATINGS; CYTOLOGY; PROTEINS; TISSUE ENGINEERING; TOPOGRAPHY;

BASEMENT MEMBRANE; CELL BEHAVIORS; CORNEAL EPITHELIAL CELLS; CORNEAL EPITHELIUM; CYTOSKELETAL DYNAMICS; CYTOSKELETAL ELEMENTS; EXTRACELLULAR MATRIX PROTEIN; TOPOGRAPHIC FEATURES;

CELL ENGINEERING;

SCLEROPROTEIN;

ARTICLE; ATOMIC FORCE MICROSCOPY; CELL CULTURE; CELL MOTION; CORNEA EPITHELIUM; CYTOLOGY; DRUG EFFECT; EPITHELIUM CELL; HUMAN; IMMUNOHISTOCHEMISTRY; DRUG EFFECTS;

CELL MOVEMENT; CELLS, CULTURED; EPITHELIAL CELLS; EPITHELIUM, CORNEAL; EXTRACELLULAR MATRIX PROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; MICROSCOPY, ATOMIC FORCE;

EID: 84879438022     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2012.0584     Document Type: Article

References (60)

1. Abrams, G.A., Goodman, S.L., Nealey, P.F., Franco, M., and Murphy, C.J. Nanoscale topography of the basement membrane underlying the corneal epithelium of the rhesus macaque. Cell Tissue Res 299, 39, 2000.
2. Abrams, G.A., Schaus, S.S., Goodman, S.L., Nealey, P.F., and Murphy, C.J. Nanoscale topography of the corneal epithelial basement Membrane and Descemet's membrane of the human. Cornea 19, 57, 2000.
3. Karuri, N.W., Porri, T.J., Albrecht, R.M., Murphy, C.J., and Nealey, P.F. Nano- and microscale holes modulate cellsubstrate adhesion, cytoskeletal organization, and -beta1 integrin localization in SV40 human corneal epithelial cells. IEEE Trans Nanobioscience 5, 273, 2006.
4. Karuri, N.W., Liliensiek, S., Teixeira, A.I., Abrams, G., Campbell, S., Nealey, P.F., and Murphy, C.J. Biological length scale topography enhances cell-substratum adhesion of human corneal epithelial cells. J Cell Sci 117(Pt15), 3153, 2004.
5. Karuri, N.W., Nealey, P.F., Murphy, C.J., and Albrecht, R.M. Structural organization of the cytoskeleton in SV40 human corneal epithelial cells cultured on nano- and microscale grooves. Scanning 30, 405, 2008.
6. Liliensiek, S.J., Wood, J.A., Yong, J., Auerbach, R., Nealey, P.F., and Murphy, C.J. Modulation of human vascular endothelial cell behaviors by nanotopographic cues. Biomaterials 31, 5418, 2010.
7. Pot, S.A., Liliensiek, S.J., Myrna, K.E., Bentley, E., Jester, J.V., Nealey, P.F., and Murphy, C.J. Nanoscale topography- induced modulation of fundamental cell behaviors of rabbit corneal keratocytes, fibroblasts, and myofibroblasts. Invest Ophthalmol Vis Sci 51, 1373, 2010.
8. Tocce, E.J., Smirnov, V.K., Kibalov, D.S., Liliensiek, S.J., Murphy, C.J., and Nealey, P.F. The ability of corneal epithelial cells to recognize high aspect ratio nanostructures. Biomaterials 31, 4064, 2010.
9. Dalby, M.J., Riehle, M.O., Yarwood, S.J., Wilkinson, C.D.W., and Curtis, A.S.G. Nucleus alignment and cell signaling in fibroblasts: response to a micro-grooved topography. Exp Cell Res 284, 272, 2003.
10. McKee Clayton, T., Raghunathan Vijay, K., Nealey Paul, F., Russell, P., and Murphy Christopher, J. Topographic modulation of the orientation and shape of cell nuclei and their influence on the measured elastic modulus of epithelial cells. Biophys J 101, 2139, 2011.
11. Morgan, J.T., Wood, J.A., Shah, N.M., Hughbanks, M.L., Russell, P., Barakat, A.I., and Murphy, C.J. Integration of basal topographic cues and apical shear stress in vascular endothelial cells. Biomaterials 33, 4126, 2012.
12. Foley, J.D., Grunwald, E.W., Nealey, P.F., and Murphy, C.J. Cooperative modulation of neuritogenesis by PC12 cells by topography and nerve growth factor. Biomaterials 26, 3639, 2005.
13. Thomasy, S.M., Wood, J.A., Kass, P.H., Murphy, C.J., and Russell, P. Substratum stiffness and latrunculin B regulate matrix gene and protein expression in human trabecular meshwork cells. Invest Ophthalmol Vis Sci 53, 952, 2012.
14. Wood, J.A., McKee, C.T., Thomasy, S.M., Fischer, M.E., Shah, N.M., Murphy, C.J., and Russell, P. Substratum compliance regulates human trabecular meshwork cell behaviors and response to latrunculin B. Invest Ophthalmol Vis Sci 52, 9298, 2011.
15. Teixeira, A.I., McKie, G.A., Foley, J.D., Bertics, P.J., Nealey, P.F., and Murphy, C.J. The effect of environmental factors on the response of human corneal epithelial cells to nanoscale substrate topography. Biomaterials 27, 3945, 2006.
16. Koo, S., Ahn, S., Zhang, H., Wang, J., and Yim, E. Human corneal keratocyte response to micro- and nano-gratings on chitosan and PDMS. Cell Mol Bioeng 4, 399, 2011.
17. Wang, G., Liu, X., Zreiqat, H., and Ding, C. Enhanced effects of nano-scale topography on the bioactivity and osteoblast behaviors of micron rough ZrO2 coatings. Colloids and Surfaces B: Biointerfaces 86, 267, 2011.
18. Sweeney, D.F., Xie, R.Z., Evans, M.D.M., Vannas, A., Tout, S.D., Griesser, H.J., Johnson, G., and Steele, J.G. A comparison of biological coatings for the promotion of corneal epithelialization of synthetic surface in vivo. Invest Ophthalmol Vis Sci 44, 3301, 2003.
19. Tocce, E.J., Broderick, A.H., Murphy, K.C., Liliensiek, S.J., Murphy, C.J., Lynn, D.M., and Nealey, P.F. Functionalization of reactive polymer multilayers with RGD and an antifouling motif: RGD density provides control over human corneal epithelial cell-substrate interactions. J Biomed Mater Res Part A 100A, 84, 2012.
20. Grohmann, S., Rothe, H., Frant, M., and Liefeith, K. Colloidal force spectroscopy and cell biological investigations on biomimetic polyelectrolyte multilayer coatings composed of chondroitin sulfate and heparin. Biomacromolecules 12, 1987, 2011.
21. van Horssen, R., Galjart, N., Rens, J.A.P., Eggermont, A.M.M., and ten Hagen, T.L.M. Differential effects of matrix and growth factors on endothelial and fibroblast motility: application of a modified cell migration assay. J Cell Biochem 99, 1536, 2006.
22. Aucoin, L., Griffith, C.M., Pleizier, G., Deslandes, Y., and Sheardown, H. Interactions of corneal epithelial cells and surfaces modified with cell adhesion peptide combinations. J Biomater Sci Polym Ed 13, 447, 2002.
23. Fong, E., Tzlil, S., and Tirrell, D.A. Boundary crossing in epithelial wound healing. Proc Natl Acad Sci U S A 107, 19302, 2010.
24. Huang, Z., Sargeant, T.D., Hulvat, J.F., Mata, A., Bringas, P., Jr., Koh, C.Y., Stupp, S.I., and Snead, M.L. Bioactive nanofibers instruct cells to proliferate and differentiate during enamel regeneration. J Bone Miner Res 23, 1995, 2008.
25. Lee, K.Y., Alsberg, E., Hsiong, S., Comisar, W., Linderman, J., Ziff, R., and Mooney, D. Nanoscale adhesion ligand organization regulates osteoblast proliferation and differentiation. Nano Lett 4, 1501, 2004.
26. Rowley, J.A., and Mooney, D.J. Alginate type and RGD density control myoblast phenotype. J Biomed Mater Res 60, 217, 2002.
27. Wang, H., Ma, L., Yang, S., Shao, Z., Meng, C., Duan, D., and Li, Y. Effect of RGD-modified silk material on the adhesion and proliferation of bone marrow-derived mesenchymal stem cells. J Huazhong Univ Sci Technolog Med Sci 29, 80, 2009.
28. Schwartz, M.A. Integrins and extracellular matrix in mechanotransduction. Cold Spring Harbor Perspect Biol 2, a005066, 2010.
29. Schwartz, M.A., and Assoian, R.K. Integrins and cell proliferation. J Cell Sci 114, 2553, 2001.
30. Myrna, K.E., Pot, S.A., and Murphy, C.J. Meet the corneal myofibroblast: The role of myofibroblast transformation in corneal wound healing and pathology. Vet Ophthalmol 12, 25, 2009.
31. Teixeira, A.I., Abrams, G.A., Bertics, P.J., Murphy, C.J., and Nealey, P.F. Epithelial contact guidance on well-defined micro- and nanostructured substrates. J Cell Sci 116, 1881, 2003.
32. Odom, T.W., Love, J.C., Wolfe, D.B., Paul, K.E., and Whitesides, G.M. Improved pattern transfer in soft lithography using composite stamps. Langmuir 18, 5314, 2002.
33. Robertson, D.M., Li, L., Fisher, S., Pearce, V.P., Shay, J.W., Wright, W.E., Cavanagh, H.D., and Jester, J.V. Characterization of growth and differentiation in a telomeraseimmortalized human corneal epithelial cell line. Invest Ophthalmol Vis Sci 46, 470, 2005.
34. Kabosova, A., Azar, D.T., Bannikov, G.A., Campbell, K.P., Durbeej, M., Ghohestani, R.F., Jones, J.C.R., Kenney, M.C., Koch, M., and Ninomiya, Y. Compositional differences between infant and adult human corneal basement membranes. Invest Ophthalmol Vis Sci 48, 4989, 2007.
35. Ljubimov, A.V., Burgeson, R.E., Butkowski, R.J., Michael, A.F., Sun, T.T., and Kenney, M.C. Human corneal basement membrane heterogeneity: topographical differences in the expression of type IV collagen and laminin isoforms. Lab Invest 72, 461, 1995
36. Madri, J.A., and Marx, M. Matrix composition, organization and soluble factors: modulators of microvascular cell differentiation in vitro. Kidney Int 41, 560, 1992.
37. Madri, J.A., Marx, M., Merwin, J.R., Basson, C., Prinz, C., and Bell, L. Effects of soluble factors and extracellular matrix components on vascular cell behavior in vitro and in vivo: models of de-endothelialization and repair. J Cell Biochem 45, 123, 1991.
38. Juliano, R. Cooperation between soluble factors and integrin-mediated cell anchorage in the control of cell growth and differentiation. Bioessays 18, 911, 1996.
39. Fraser, S.A., Ting, Y.-H., Mallon, K.S., Wendt, A.E., Murphy, C.J., and Nealey, P.F. Sub-micron and nanoscale feature depth modulates alignment of stromal fibroblasts and corneal epithelial cells in serum-rich and serum-free media. J Biomed Mater Res Part A 86A, 725, 2008.
40. Healy, K.E., Thomas, C.H., Rezania, A., Kim, J.E., McKeown, P.J., Lom, B., and Hockberger, P.E. Kinetics of bone cell organization and mineralization on materials with patterned surface chemistry. Biomaterials 17, 195, 1996.
41. Anselme, K., Linez, P., Bigerelle, M., Le Maguer, D., Le Maguer, A., Hardouin, P., Hildebrand, H.F., Iost, A., and Leroy, J.M. The relative influence of the topography and chemistry of TiAl6V4 surfaces on osteoblastic cell behaviour. Biomaterials 21, 1567, 2000.
42. Mrksich, M. A surface chemistry approach to studying cell adhesion. Chem Soc Rev 29, 267, 2000.
43. Stevens, M.M., and George, J.H. Exploring and engineering the cell surface interface. Science 310, 1135, 2005.
44. Marois, Y., Sugot-Luizard, M.F., and Guidoin, R. Endothelial cell behavior on vascular prosthetic grafts: effect of polymer chemistry, surface structure, and surface treatment. ASAIO J 45, 272, 1999.
45. Ponsonnet, L., Reybier, K., Jaffrezic, N., Comte, V., Lagneau, C., Lissac, M., and Martelet, C. Relationship between surface properties (roughness, wettability) of titanium and titanium alloys and cell behaviour. Mater Sci Eng C 23, 551, 2003.
46. Deligianni, D.D., Katsala, N.D., Koutsoukos, P.G., and Missirlis, Y.F. Effect of surface roughness of hydroxyapatite on human bone marrow cell adhesion, proliferation, differentiation and detachment strength. Biomaterials 22, 87, 2000.
47. Hallab, N.J., Bundy, K.J., O'Connor, K., Moses, R.L., and Jacobs, J.J. Evaluation of metallic and polymeric biomaterial surface energy and surface roughness characteristics for directed cell adhesion. Tissue Eng 7, 55, 2001.
48. Xu, C., Yang, F., Wang, S., and Ramakrishna, S. In vitro study of human vascular endothelial cell function on materials with various surface roughness. J Biomed Mater Res Part A 71A, 154, 2004.
49. Houtchens, G.R., Foster, M.D., Desai, T.A., Morgan, E.F., and Wong, J.Y. Combined effects of microtopography and cyclic strain on vascular smooth muscle cell orientation. J Biomech 41, 762, 2008.
50. Wilson, M.J., Liliensiek, S.J., Murphy, C.J., Murphy, W.L., and Nealey, P.F. Hydrogels with well-defined peptidehydrogel spacing and concentration: impact on epithelial cell behavior. Soft Matter 8, 390, 2012.
51. Fujikawa, L.S., Foster, C.S., Gipson, I.K., and Colvin, R.B. Basement membrane components in healing rabbit corneal epithelial wounds: immunofluorescence and ultrastructural studies. J Cell Biol 98, 128, 1984.
52. Nishida, T., Nakagawa, S., Awata, T., Ohashi, Y., Watanabe, K., and Manabe, R. Fibronectin promotes epithelial migration of cultured rabbit cornea in situ. J Cell Biol 97, 1653, 1983.
53. Watanabe, K., Nakagawa, S., and Nishida, T. Stimulatory effects of fibronectin and EGF on migration of corneal epithelial cells. Invest Ophthalmol Vis Sci 28, 205, 1987.
54. Diehl, K.A., Foley, J.D., Nealey, P.F., and Murphy, C.J. Nanoscale topography modulates corneal epithelial cell migration. J Biomed Mater Res Part A 75A, 603, 2005.
55. Ridley, A.J., Schwartz, M.A., Burridge, K., Firtel, R.A., Ginsberg, M.H., Borisy, G., Parsons, J.T., and Horwitz, A.R. Cell migration: integrating signals from front to back. Science 302, 1704, 2003.
56. Gasiorowski, J.Z., Liliensiek, S.J., Russell, P., Stephan, D.A., Nealey, P.F., and Murphy, C.J. Alterations in gene expression of human vascular endothelial cells associated with nanotopographic cues. Biomaterials 31, 8882, 2010.
57. Yim, E.K.F., and Leong, K.W. Significance of synthetic nanostructures in dictating cellular response. Nanomedicine 1, 10, 2005.
58. Schoenwaelder, S.M., and Burridge, K. Bidirectional signaling between the cytoskeleton and integrins. Curr Opin Cell Biol 11, 274, 1999.
59. Dahl, K.N., Ribeiro, A.J.S., and Lammerding, J. Nuclear shape, mechanics, and mechanotransduction. Circ Res 102, 1307, 2008.
60. Hoshiba, T., Yamada, T., Lu, H., Kawazoe, N., Tateishi, T., and Chen, G. Nuclear deformation and expression change of cartilaginous genes during in vitro expansion of chondrocytes. Biochem Biophys Res Commun 374, 688, 2008.