Focal adhesion kinase knockdown modulates the response of human corneal epithelial cells to topographic cues

Acta Biomaterialia

Volumn 8, Issue 12, 2012, Pages 4285-4294

  Dreier, Britta ^a   Raghunathan, Vijaya Krishna ^a   Russell, Paul ^a   Murphy, Christopher J ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Biomimetic material; Cell signaling; Cornea; Focal adhesion kinase; Nanotopography

Indexed keywords

ADHESION; BIOMIMETIC MATERIALS; BIOMIMETICS; CYTOLOGY; ENZYMES; GENE EXPRESSION; MOLECULAR BIOLOGY;

CELLULAR BEHAVIORS; CORNEA; FOCAL ADHESION KINASE; HUMAN CORNEAL; HUMAN CORNEAL EPITHELIAL CELLS; LONG AXIS; MECHANOTRANSDUCTION; NANOTOPOGRAPHIES; RESEARCH EFFORTS; SIGNALING PROCESS;

CELL SIGNALING;

FOCAL ADHESION KINASE;

ARTICLE; CELL MIGRATION; CELL SIZE; CONTROLLED STUDY; CORNEA EPITHELIUM; ENZYME LOCALIZATION; EPITHELIUM CELL; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; PRIORITY JOURNAL;

EID: 84868197336     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2012.07.004     Document Type: Article

References (63)

1. J.P. Whitcher, M. Srinivasan, and M.P. Upadhyay Corneal blindness: a global perspective Bull World Health Org 79 2001 214 221 (Pubitemid 32246479)
2. G.A. Abrams, E. Bentley, P.F. Nealey, and C.J. Murphy Electron microscopy of the canine corneal basement membranes Cells Tissues Organs 170 2002 251 257 (Pubitemid 34264166)
3. G.A. Abrams, S.S. Schaus, S.L. Goodman, P.F. Nealey, and C.J. Murphy Nanoscale topography of the corneal epithelial basement membrane and Descemet's membrane of the human Cornea 19 2000 57 64 (Pubitemid 30007746)
4. J.A. Last, S.J. Liliensiek, P.F. Nealey, and C.J. Murphy Determining the mechanical properties of human corneal basement membranes with atomic force microscopy J Struct Biol 167 2009 19 24
5. N.W. Karuri, T.J. Porri, R.M. Albrecht, C.J. Murphy, and P.F. Nealey Nano- and microscale holes modulate cell-substrate adhesion, cytoskeletal organization, and -beta1 integrin localization in SV40 human corneal epithelial cells IEEE Trans Nanobiosci 5 2006 273 280 (Pubitemid 44955828)
6. N.W. Karuri, S. Liliensiek, A.I. Teixeira, G. Abrams, S. Campbell, and P.F. Nealey Biological length scale topography enhances cell-substratum adhesion of human corneal epithelial cells J Cell Sci 117 2004 3153 3164 (Pubitemid 39139902)
7. S.J. Liliensiek, S. Campbell, P.F. Nealey, and C.J. Murphy The scale of substratum topographic features modulates proliferation of corneal epithelial cells and corneal fibroblasts J Biomed Mater Res Part A 79 2006 185 192 (Pubitemid 44452869)
8. K.A. Owen, M.Y. Abshire, R.W. Tilghman, J.E. Casanova, and A.H. Bouton FAK regulates intestinal epithelial cell survival and proliferation during mucosal wound healing PLoS One 6 2011 e23123
9. K.A. Diehl, J.D. Foley, P.F. Nealey, and C.J. Murphy Nanoscale topography modulates corneal epithelial cell migration J Biomed Mater Res Part A 75 2005 603 611 (Pubitemid 47233444)
10. S.A. Pot, S.J. Liliensiek, K.E. Myrna, E. Bentley, J.V. Jester, and P.F. Nealey Nanoscale topography-induced modulation of fundamental cell behaviors of rabbit corneal keratocytes, fibroblasts, and myofibroblasts Invest Ophthalmol Vis Sci 51 2010 1373 1381
11. A.I. Teixeira, G.A. Abrams, P.J. Bertics, C.J. Murphy, and P.F. Nealey Epithelial contact guidance on well-defined micro- and nanostructured substrates J Cell Sci 116 2003 1881 1892 (Pubitemid 36622287)
12. A.I. Teixeira, G.A. McKie, J.D. Foley, P.J. Bertics, P.F. Nealey, and C.J. Murphy The effect of environmental factors on the response of human corneal epithelial cells to nanoscale substrate topography Biomaterials 27 2006 3945 3954
13. A.I. Teixeira, P.F. Nealey, and C.J. Murphy Responses of human keratocytes to micro- and nanostructured substrates J Biomed Mater Res Part A 71 2004 369 376 (Pubitemid 39488509)
14. E.J. Tocce, V.K. Smirnov, D.S. Kibalov, S.J. Liliensiek, C.J. Murphy, and P.F. Nealey The ability of corneal epithelial cells to recognize high aspect ratio nanostructures Biomaterials 31 2010 4064 4072
15. S.K. Hanks, M.B. Calalb, M.C. Harper, and S.K. Patel Focal adhesion protein-tyrosine kinase phosphorylated in response to cell attachment to fibronectin Proc Natl Acad Sci USA 89 1992 8487 8491
16. M.D. Schaller, C.A. Otey, J.D. Hildebrand, and J.T. Parsons Focal adhesion kinase and paxillin bind to peptides mimicking beta integrin cytoplasmic domains J Cell Biol 130 1995 1181 1187
17. M.D. Schaller, J.D. Hildebrand, J.D. Shannon, J.W. Fox, R.R. Vines, and J.T. Parsons Autophosphorylation of the focal adhesion kinase, pp 125FAK, directs SH2-dependent binding of pp60src Mol Cell Biol 14 1994 1680 1688
18. M.C. Brown, J.A. Perrotta, and C.E. Turner Identification of LIM3 as the principal determinant of paxillin focal adhesion localization and characterization of a novel motif on paxillin directing vinculin and focal adhesion kinase binding J Cell Biol 135 1996 1109 1123 (Pubitemid 26403782)
19. J.D. Hildebrand, M.D. Schaller, and J.T. Parsons Paxillin, a tyrosine phosphorylated focal adhesion-associated protein binds to the carboxyl terminal domain of focal adhesion kinase Mol Biol Cell 6 1995 637 647
20. C.E. Turner, and J.T. Miller Primary sequence of paxillin contains putative SH2 and SH3 domain binding motifs and multiple LIM domains: identification of a vinculin and pp 125Fak-binding region J Cell Sci 107 Pt 6 1994 1583 1591
21. H.C. Chen, P.A. Appeddu, J.T. Parsons, J.D. Hildebrand, M.D. Schaller, and J.L. Guan Interaction of focal adhesion kinase with cytoskeletal protein talin J Biol Chem 270 1995 16995 16999
22. L.A. Cary, D.C. Han, T.R. Polte, S.K. Hanks, and J.L. Guan Identification of p130Cas as a mediator of focal adhesion kinase-promoted cell migration J Cell Biol 140 1998 211 221 (Pubitemid 28070908)
23. B.S. Cobb, M.D. Schaller, T.H. Leu, and J.T. Parsons Stable association of pp 60src and pp59fyn with the focal adhesion-associated protein tyrosine kinase, pp125FAK Mol Cell Biol 14 1994 147 155
24. D.D. Schlaepfer, S.K. Mitra, and D. Ilic Control of motile and invasive cell phenotypes by focal adhesion kinase Biochim Biophys Acta 1692 2004 77 102 (Pubitemid 38898737)
25. J. Zhao, C. Zheng, and J. Guan Pyk2 and FAK differentially regulate progression of the cell cycle J Cell Sci 113 Pt 17 2000 3063 3072
26. J.H. Zhao, H. Reiske, and J.L. Guan Regulation of the cell cycle by focal adhesion kinase J Cell Biol 143 1998 1997 2008 (Pubitemid 29022619)
27. Q. Lu, and S. Rounds Focal adhesion kinase and endothelial cell apoptosis Microvasc Res 83 2012 56 63
28. D. Ilic, Y. Furuta, S. Kanazawa, N. Takeda, K. Sobue, and N. Nakatsuji Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice Nature 377 1995 539 544
29. H.B. Wang, M. Dembo, S.K. Hanks, and Y. Wang Focal adhesion kinase is involved in mechanosensing during fibroblast migration Proc Natl Acad Sci USA 98 2001 11295 11300 (Pubitemid 32928722)
30. M. Dreger, L. Bengtsson, T. Schoneberg, H. Otto, and F. Hucho Nuclear envelope proteomics: novel integral membrane proteins of the inner nuclear membrane Proc Natl Acad Sci USA 98 2001 11943 11948 (Pubitemid 32959806)
31. V.C. Padmakumar, T. Libotte, W. Lu, H. Zaim, S. Abraham, and A.A. Noegel The inner nuclear membrane protein Sun1 mediates the anchorage of Nesprin-2 to the nuclear envelope J Cell Sci 118 2005 3419 3430 (Pubitemid 41246097)
32. H.J. Worman, and G.G. Gundersen Here come the SUNs: a nucleocytoskeletal missing link Trends Cell Biol 16 2006 67 69 (Pubitemid 43247401)
33. J. Lammerding, P.C. Schulze, T. Takahashi, S. Kozlov, T. Sullivan, and R.D. Kamm Lamin A/C deficiency causes defective nuclear mechanics and mechanotransduction J Clin Invest 113 2004 370 378 (Pubitemid 38544181)
34. J. Lammerding, J. Hsiao, P.C. Schulze, S. Kozlov, C.L. Stewart, and R.T. Lee Abnormal nuclear shape and impaired mechanotransduction in emerin-deficient cells J Cell Biol 170 2005 781 791 (Pubitemid 41242110)
35. D.A. Starr, and M. Han Role of ANC-1 in tethering nuclei to the actin cytoskeleton Science 298 2002 406 409 (Pubitemid 35176347)
36. Q. Zhang, C. Bethmann, N.F. Worth, J.D. Davies, C. Wasner, and A. Feuer Nesprin-1 and -2 are involved in the pathogenesis of Emery Dreifuss muscular dystrophy and are critical for nuclear envelope integrity Hum Mol Genet 16 2007 2816 2833 (Pubitemid 350048381)
37. T.J. Chancellor, J. Lee, C.K. Thodeti, and T. Lele Actomyosin tension exerted on the nucleus through nesprin-1 connections influences endothelial cell adhesion, migration, and cyclic strain-induced reorientation Biophys J 99 2010 115 123
38. Q. Zhang, C. Ragnauth, M.J. Greener, C.M. Shanahan, and R.G. Roberts The nesprins are giant actin-binding proteins, orthologous to Drosophila melanogaster muscle protein MSP-300 Genomics 80 2002 473 481 (Pubitemid 35333789)
39. E.D. Apel, R.M. Lewis, R.M. Grady, and J.R. Sanes Syne-1, a dystrophin- and Klarsicht-related protein associated with synaptic nuclei at the neuromuscular junction J Biol Chem 275 2000 31986 31995
40. J.M. Mislow, M.S. Kim, D.B. Davis, and E.M. McNally Myne-1, a spectrin repeat transmembrane protein of the myocyte inner nuclear membrane, interacts with lamin A/C J Cell Sci 115 2002 61 70 (Pubitemid 34105529)
41. Q. Zhang, C.D. Ragnauth, J.N. Skepper, N.F. Worth, D.T. Warren, and R.G. Roberts Nesprin-2 is a multi-isomeric protein that binds lamin and emerin at the nuclear envelope and forms a subcellular network in skeletal muscle J Cell Sci 118 2005 673 687 (Pubitemid 40372577)
42. D.T. Warren, T. Tajsic, J.A. Mellad, R. Searles, Q. Zhang, and C.M. Shanahan Novel nuclear nesprin-2 variants tether active extracellular signal-regulated MAPK1 and MAPK2 at promyelocytic leukemia protein nuclear bodies and act to regulate smooth muscle cell proliferation J Biol Chem 285 2010 1311 1320
43. D.J. Webb, K. Donais, L.A. Whitmore, S.M. Thomas, C.E. Turner, and J.T. Parsons FAK-Src signalling through paxillin, ERK and MLCK regulates adhesion disassembly Nat Cell Biol 6 2004 154 161 (Pubitemid 38425715)
44. T.W. Odom, J.C. Love, D.B. Wolfe, K.E. Paul, and G.M. Whitesides Improved pattern transfer in soft lithography using composite stamps Langmuir 18 2002 5314 5320 (Pubitemid 35383515)
45. S.J. Liliensiek, J.A. Wood, J. Yong, R. Auerbach, P.F. Nealey, and C.J. Murphy Modulation of human vascular endothelial cell behaviors by nanotopographic cues Biomaterials 31 2010 5418 5426
46. Clayton T. McKee, Vijay K. Raghunathan, Paul F. Nealey, P. Russell, and Christopher J. Murphy Topographic modulation of the orientation and shape of cell nuclei and their influence on the measured elastic modulus of epithelial cells Biophys J 101 2011 2139 2146
47. D.M. Robertson, L. Li, S. Fisher, V.P. Pearce, J.W. Shay, and W.E. Wright Characterization of growth and differentiation in a telomerase-immortalized human corneal epithelial cell line Invest Ophthalmol Vis Sci 46 2005 470 478 (Pubitemid 40270324)
48. S.A. Fraser, Y.H. Ting, K.S. Mallon, A.E. Wendt, C.J. Murphy, and P.F. Nealey 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 86 2008 725 735
49. J.Z. Gasiorowski, S.J. Liliensiek, P. Russell, D.A. Stephan, P.F. Nealey, and C.J. Murphy Alterations in gene expression of human vascular endothelial cells associated with nanotopographic cues Biomaterials 31 2010 8882 8888
50. E.K. Yim, E.M. Darling, K. Kulangara, F. Guilak, and K.W. Leong Nanotopography-induced changes in focal adhesions, cytoskeletal organization, and mechanical properties of human mesenchymal stem cells Biomaterials 31 2010 1299 1306
51. J.Y. Lim, A.D. Dreiss, Z. Zhou, J.C. Hansen, C.A. Siedlecki, and R.W. Hengstebeck The regulation of integrin-mediated osteoblast focal adhesion and focal adhesion kinase expression by nanoscale topography Biomaterials 28 2007 1787 1797 (Pubitemid 46137997)
52. E.T. Den Braber, J.E. de Ruijter, H.T.J. Smits, L.A. Ginsel, A.F. von Recum, and J.A. Jansen Effect of parallel surface microgrooves and surface energy on cell growth J Biomed Mater Res 29 1995 511 518
53. M.T. Frey, I.Y. Tsai, T.P. Russell, S.K. Hanks, and Y.L. Wang Cellular responses to substrate topography: role of myosin II and focal adhesion kinase Biophys J 90 2006 3774 3782
54. T. Molina, K. Kabsch, A. Alonso, A. Kohl, G. Komposch, and P. Tomakidi Topographic changes of focal adhesion components and modulation of p125FAK activation in stretched human periodontal ligament fibroblasts J Dent Res 80 2001 1984 1989
55. E.A. Klein, L. Yin, D. Kothapalli, P. Castagnino, F.J. Byfield, and T. Xu Cell-cycle control by physiological matrix elasticity and in vivo tissue stiffening Curr Biol 19 2009 1511 1518
56. L.S. Fujikawa, C.S. Foster, I.K. Gipson, and R.B. Colvin Basement membrane components in healing rabbit corneal epithelial wounds: immunofluorescence and ultrastructural studies J Cell Biol 98 1984 128 138 (Pubitemid 14220474)
57. S.E. Wilson, R.R. Mohan, R. Ambrosio Jr., J. Hong, and J. Lee The corneal wound healing response: cytokine-mediated interaction of the epithelium, stroma, and inflammatory cells Prog Retin Eye Res 20 2001 625 637 (Pubitemid 32695343)
58. A.P. Gilmore, and L.H. Romer Inhibition of focal adhesion kinase (FAK) signaling in focal adhesions decreases cell motility and proliferation Mol Biol Cell 7 1996 1209 1224 (Pubitemid 26260738)
59. D.J. Sieg, C.R. Hauck, and D.D. Schlaepfer Required role of focal adhesion kinase (FAK) for integrin-stimulated cell migration J Cell Sci 112 Pt 16 1999 2677 2691 (Pubitemid 29429791)
60. A.K. Sood, J.E. Coffin, G.B. Schneider, M.S. Fletcher, B.R. DeYoung, and L.M. Gruman Biological significance of focal adhesion kinase in ovarian cancer: role in migration and invasion Am J Pathol 165 2004 1087 1095 (Pubitemid 39297716)
61. L.A. Cary, J.F. Chang, and J.L. Guan Stimulation of cell migration by overexpression of focal adhesion kinase and its association with Src and Fyn J Cell Sci 109 Pt 7 1996 1787 1794 (Pubitemid 26248624)
62. A. Tomar, and D.D. Schlaepfer Focal adhesion kinase: switching between GAPs and GEFs in the regulation of cell motility Curr Opin Cell Biol 21 2009 676 683
63. S.K. Mitra, D.A. Hanson, and D.D. Schlaepfer Focal adhesion kinase: in command and control of cell motility Nat Rev Mol Cell Biol 6 2005 56 68 (Pubitemid 40064899)