Mechanical interactions and crosstalk between corneal keratocytes and the extracellular matrix

Experimental Eye Research

Volumn 133, Issue , 2015, Pages 49-57

  Petroll, W Matthew ^a   Miron Mendoza, Miguel ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Cell mechanics; Corneal keratocytes; Corneal stroma; Extracellular matrix; Mechanobiology

Indexed keywords

GROWTH FACTOR; RAC PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHO KINASE;

ADULT CORNEAL STROMAL STEM CELL; ADULT STEM CELL; ANISOTROPY; BIOCHEMICAL COMPOSITION; BIOPHYSICS; CELL DIFFERENTIATION; CELL INTERACTION; CELL MIGRATION; CELL MOTILITY; CELL SPREADING; CELL STRESS; CELL STRUCTURE; CORNEA CELL; CORNEA INJURY; CORNEA STROMA CELL; CROSS LINKING; EXTRACELLULAR MATRIX; FEEDBACK SYSTEM; HUMAN; MECHANICS; MECHANOTRANSDUCTION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; RIGIDITY; WOUND HEALING; BIOMECHANICS; CELL COMMUNICATION; CONFOCAL MICROSCOPY; CORNEA STROMA; CYTOLOGY; METABOLISM; PHYSIOLOGY;

BIOMECHANICAL PHENOMENA; CELL COMMUNICATION; CORNEAL KERATOCYTES; CORNEAL STROMA; EXTRACELLULAR MATRIX; HUMANS; MICROSCOPY, CONFOCAL;

EID: 84925382251     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2014.09.003     Document Type: Review

References (131)

1. Ali N.Q., Patel D.V., McGhee C.N. Biomechanical responses of healthy and keratoconic corneas measured using a noncontact scheimpflug-based tonometer. Invest Ophthalmol. Vis. Sci. 2014, 55:3651-3659.
2. Amano M., Chihara K., Nakamura N., Fukata Y., Yano T., Shibata M., Ikebe M., Kaibuchi K. Myosin II activation promotes neurite retraction during the action of Rho and Rho-kinase. Genes Cells 1998, 3:177-188.
3. Amano M., Ito M., Kimura K., Fukata Y., Chihara K., Nakano T., Matsuura Y., Kaibuchi K. Phosphorylation and activation of myosin by Rho-associated kinase (Rho-kinase). J.Biol. Chem. 1996, 271:20246-20249.
4. Amano M., Nakayama M., Kaibuchi K. Rho-kinase/ROCK: a key regulator of the cytoskeleton and cell polarity. Cytoskelet. Hob. 2010, 67:545-554.
5. Ambekar R., Toussaint K.C., Wagoner Johnson A. The effect of keratoconus on the structural, mechanical, and optical properties of the cornea. J.Mech. Behav. Biomed. Mater. 2011, 4:223-236.
6. Anderson S., DiCesare L., Tan I., Leung T., SundarRaj N. Rho-mediated assembly of stress fibers is differentially regulated in corneal fibroblats and myofibroblasts. Exp. Cell. Res. 2004, 298:574-583.
7. Andreassen T.T., Simonsen A.H., Oxlund H. Biomechanical properties of keratoconus and normal corneas. Exp. Eye Res. 1980, 31:435-441.
8. Andresen J.L., Ledet T., Ehlers N. Keratocyte migration and peptide growth factors: the effect of PDGF, bFGF, EGF, IGF-1, aFGF and TGF-beta on human keratocyte migration in a collagen gel. Curr. Eye Res. 1997, 16:605-613.
9. Bard J.B.L., Higginson K. Fibroblast-collagen interactions in the formation of the secondary stroma of the chick cornea. J.Cell. Biol. 1977, 74:816-827.
10. Berthaut A., Mirshahi P., Benabbou N., Ducros E., Agra A., Therwath A., Legeais J.M., Mirshahi M. Insulin growth factor promotes human corneal fibroblast network formation invitro. Invest Ophthalmol. Vis. Sci. 2011, 52:7647-7653.
11. Beshtawi I.M., O'Donnell C., Radhakrishnan H. Biomechanical properties of corneal tissue after ultraviolet-A-riboflavin crosslinking. J.Cataract. Refract Surg. 2013, 39:451-462.
12. Blalock T.D., Duncan M.R., Varela J.C., Goldstein M.H., Tuli M.H., Grotensdorst G.R., Schultz G.S. Connective tissue growth factor expression and action in human corneal fibroblast cultures and rat corneas after photorefractive keratectomy. Invest. Ophthalmol. Vis. Sci. 2003, 44:1879-1887.
13. Boote C., Du Y., Morgan S., Harris J., Kamma-Lorger C., Hayes S., Lathrop K., Rob D., Burrow M., Hiller J., Terrill N., Funderburgh J., Meek K. Quantitative assessment of ultrastructure and light scatter in mouse corneal debridement wounds. Invest. Ophthalmol. Vis. Sci. 2012, 53:2786-2795.
14. Brown R.A., Prajapati R., McGrouther D.A., Yannas I.V., Eastwood M. Tensional homeostasis in dermal fibroblasts: mechanical responses to mechanical loading in three-dimensional substrates. J.Cell. Physiol. 1998, 175:323-332.
15. Brown T.D. Techniques for mechanical stimulation of cells invitro: a review. J.Biomech. 2000, 33:3-14.
16. Chakravarti S., Petroll W.M., Hassell J., Jester J.V., Lass J.H., Paul J., Birk D.E. Corneal opacity in lumican-null mice: defects in collagen fibril structure and packing in the posterior stroma. Invest. Ophthalmol. Vis. Sci. 2000, 41:3365-3373.
17. Chan A.A., Hertsenberg A.J., Funderburgh M.L., Mann M.M., Du Y., Davoli K.A., Mich-Basso J.D., Yang L., Funderburgh J.L. Differentiation of human embryonic stem cells into cells with corneal keratocyte phenotype. PLoS One 2013, 8:e56831.
18. Cheema U., Yang S.-Y., Mudera V., Goldspink G.G., Brown R.A. 3-D invitro model of early skeletal muscle development. Cell. Motil. Cytoskel. 2003, 54:226-236.
19. Chen J., Guerriero E., Sado Y., SundarRaj N. Rho-mediated regulation of TGF-beta1- and FGF-2-induced activation of corneal stromal keratocytes. Invest. Ophthalmol. Vis. Sci. 2009, 50:3662-3670.
20. Chrzanowska-Wodnicka C., Burridge K. Tyrosine phosphorylation is involved in reorganization of the actin cytoskeleton in response to serum or LPA stimulation. J.Cell. Sci. 1994, 107:3564-3643.
21. Demali K.A., Burridge K. Coupling membrane protrusion and cell adhesion. J.Cell. Sci. 2003, 116:2389-2397.
22. Dreier B., Thomasy S.M., Mendonsa R., Raghunathan V.K., Russell P., Murphy C.J. Substratum compliance modulates corneal fibroblast to myofibroblast transformation. Invest. Ophthalmol. Vis. Sci. 2013, 54:5901-5907.
23. Du Y., Funderburgh M.L., Mann M.M., SundarRaj N., Funderburgh J.L. Multipotent stem cells in human corneal stroma. Stem Cells 2005, 23:1266-1275.
24. Du Y., SundarRaj N., Funderburgh M.L., Harvey S.A., Birk D.E., Funderburgh J.L. Secretion and organization of a cornea-like tissue invitro by stem cells from human corneal stroma. Invest. Ophthalmol. Vis. Sci. 2007, 48:5038-5045.
25. Dupps W.J., Wilson S.E. Biomechanics and wound healing in the cornea. Exp. Eye Res. 2006, 83:709-720.
26. Eastwood M., McGrouther D.A., Brown R.A. Aculture force monitor for measurement of contraction forces generated in human dermal fibroblast cultures: evidence for cell matrix mechanical signalling. Biochim. Biophys. Acta 1994, 1201:186-192.
27. Eastwood M., Mudera V.C., McGrouther D.A., Brown R.A. Effect of precise mechanical loading on fibroblast populated collagen lattices: morphological changes. Cell. Motil. Cytoskel. 1998, 40:13-21.
28. Edmund C. Corneal topography and elasticity in normal and keratoconic eyes. A methodological study concerning the pathogenesis of keratoconus. Acta Ophthalmol. Suppl. 1989, 193:1-36.
29. Engler A.J., Sen S., Sweeney H.L., Discher D.E. Matrix elasticity directs stem cell lineage specification. Cell 2006, 126:677-689.
30. Etheredge L., Kane B.P., Hassell J.R. The effect of growth factor signaling on keratocytes invitro and its relationship to the phases of stromal wound repair. Invest. Ophthalmol. Vis. Sci. 2009, 50:3128-3136.
31. Frey M.T., Tsai I.Y., Russell T.P., Hanks S.K., Wang Y.L. Cellular responses to substrate topography: role of myosin II and focal adhesion kinase. Biophys. J. 2006, 90:3774-3782.
32. Freyman T.M., Yannas I.V., Yokoo R., Gibson L.J. Fibroblast contractile force is independent of the stiffness which resists the contraction. Exp. Cell. Res. 2002, 272:153-162.
33. Funderburgh J.L., Mann M.M., Funderburgh M.L. Keratocyte phenotype mediates proteoglycan structure: a role for fibroblasts in corneal fibrosis. J.Biol. Chem. 2003, 278:45629-45637.
34. Garana R.M., Petroll W.M., Chen W.T., Herman I.M., Barry P., Andrews H.D., Cavanagh H.D., Jester J.V. Radial keratotomy II: the role of the myofibroblast in corneal wound contraction. Invest. Ophthalmol. Vis. Sci. 1992, 33:3271-3282.
35. Garrett Q., Khaw P.T., Blalock T.D., Schultz G.S., Grotensdorst G.R., Daniels J.T. Involvement of CTGF in TGF-beta-1-stimulation of myofibroblast differentiation and collagen matrix contraction in the presence of mechanical stress. Invest. Ophthalmol. Vis. Sci. 2004, 45:1109-1116.
36. Ghibaudo M., Trichet L., Le Digabel J., Richert A., Hersen P., Ladoux B. Substrate topography induces a crossover from 2D to 3D behavior in fibroblast migration. Biophys. J. 2009, 97:357-368.
37. Grinnell F. Fibroblast-collagen-matrix contraction: growth-factor signalling and mechanical loading. Trends Cell. Biol. 2000, 10:362-365.
38. Grinnell F., Petroll W.M. Cell motility and mechanics in three-dimensional collagen matrices. Annu. Rev. Cell. Dev. Biol. 2010, 26:335-361.
39. Grinnell F., Rocha L.B., Iucu C., Rhee S., Jiang H. Nested collagen matrices: a new model to study migration of human fibroblast populations in three dimensions. Exp. Cell. Res. 2006, 312:86-94.
40. Guillemette M.D., Cui B., Roy E., Gauvin R., Giasson C.J., Esch M.B., Carrier P., Deschambeault A., Dumoulin M., Toner M., Germain L., Veres T., Auger F.A. Surface topography induces 3D self-orientation of cells and extracellular matrix resulting in improved tissue function. Integr. Biol. (Camb.) 2009, 1:196-204.
41. Guo X.Q., Hutcheon A.E., Melotti S.A., Zieske J.D., Trinkaus-Randall V., Ruberti J.W. Morphologic characterization of organized extracellular matrix deposition by ascorbic acid-stimulated human corneal fibroblasts. Invest. Ophthalmol. Vis. Sci. 2007, 48:4056-4060.
42. Hadjipanayi E., Mudera V., Brown R.A. Guding cell migration in 3D: a collagen matrix with graded directional stiffness. Cell. Motil. Cytoskel. 2009, 66:121-129.
43. Hall A. Rho GTPases and the control of cell behaviour. Biochem. Soc. Trans. 2005, 33:891-895.
44. Hassell J.R., Birk D.E. The molecular basis of corneal transparency. Exp. Eye Res. 2010, 91:326-335.
45. Hay E.D. Interaction of migrating embryonic cells with extracellular matrix. Exp. Biol. Med. 1985, 10:174-193.
46. He Y., Grinnell F. Stress relaxation of fibroblasts activates a cyclic AMP signaling pathway. J.Cell. Biol. 1994, 126:457-464.
47. Huang D., Chang T.R., Aggarwal A., Lee R.C., Ehrlich H.P. Mechanisms and dynamics of mechanical strengthening in ligament-equivalent fibroblast populated collagen matrices. Ann. Biomed. Eng. 1993, 21:289-305.
48. Ingber D.E., Folkman J. Mechanochemical switching between growth and differentiation during fibroblast growth factor stimulated angiogenesis invitro: role of extracellular matrix. J.Cell. Biol. 1989, 109:317-330.
49. Inoue T., Tanihara H. Rho-associated kinase inhibitors: a novel glaucoma therapy. Prog. Retin Eye Res. 2013, 37:1-12.
50. Jaffe A.B., Hall A. Rho GTPases: biochemistry and biology. Annu. Rev. Cell. Dev. Biol. 2005, 21:247-269.
51. Jester J.V., Barry P.A., Lind G.J., Petroll W.M., Garana R., Cavanagh H.D. Corneal keratocytes: in situ and invitro organization of cytoskeletal contractile proteins. Invest. Ophthalmol. Vis. Sci. 1994, 35:730-743.
52. Jester J.V., Brown D., Pappa A., Vasilou V. Myofibroblast differentiation modulates keratocyte crystallin protein expression, concentration, and cellular light scattering. Invest. Ophthalmol. Vis. Sci. 2012, 53:770-778.
53. Jester J.V., Chang J.-H. Modulation of cultured corneal keratocyte phenotype by growth factors/cytokines control invitro contractility and extracellular matrix contraction. Exp. Eye Res. 2003, 77:581-592.
54. Jester J.V., Huang J., Barry-Lane P.A., Kao W.W., Petroll W.M., Cavanagh H.D. Transforming growth factor(beta)-mediated corneal myofibroblast differentiation requires actin and fibronectin assembly. Invest. Ophthalmol. Vis. Sci. 1999, 40:1959-1967.
55. Jester J.V., Huang J., Petroll W.M., Cavanagh H.D. TGFbeta induced myofibroblast differentiation of rabbit keratocytes requires synergistic TGFbeta, PDGF and integrin signalling. Exp. Eye Res. 2002, 75:645-657.
56. Jester J.V., Petroll W.M., Cavanagh H.D. Corneal stromal wound healing in refractive surgery: the role of the myofibroblast. Prog. Retin. Eye Res. 1999, 18:311-356.
57. Karamichos D., Funderburgh M.L., Hutcheon A.E., Zieske J.D., Du Y., Wu J., Funderburgh J.L. Arole for topographic cues in the organization of collagenous matrix by corneal fibroblasts and stem cells. PLoS One 2014, 9:e86260.
58. Karamichos D., Guo X.Q., Hutcheon A.E., Zieske J.D. Human corneal fibrosis: an invitro model. Invest. Ophthalmol. Vis. Sci. 2010, 51:1382-1388.
59. Karamichos D., Lakshman N., Petroll W.M. Regulation of corneal fibroblast morphology and collagen reorganization by extracellular matrix mechanical properties. Invest. Ophthalmol. Vis. Sci. 2007, 48:5030-5037.
60. Karamichos D., Lakshman N., Petroll W.M. An experimental model for assessing fibroblast migration in 3-D collagen matrices. Cell. Motil. Cytoskel. 2009, 66:1-9.
61. Kim A., Lakshman N., Karamichos D., Petroll W.M. Growth factor regulation of corneal keratocyte differentiation and migration in compressed collagen matrices. Invest. Ophthalmol. Vis. Sci. 2010, 51:864-875.
62. Kim A., Lakshman N., Petroll W.M. Quantitative assessment of local collagen matrix remodeling in 3-D culture: the role of Rho kinase. Exp. Cell. Res. 2006, 312:3683-3692.
63. Kim A., Zhou C., Lakshman N., Petroll W.M. Corneal stromal cells use both high- and low-contractility migration mechanisms in 3-D collagen matrices. Exp. Cell. Res. 2012, 318:741-752.
64. Kim D.H., Provenzano P.P., Smith C.L., Levchenko A. Matrix nanotopography as a regulator of cell function. J.Cell. Biol. 2012, 197:351-360.
65. Kimura K., Ito M., Amano M., Chihara K., Fukuta Y., Nakafuku M., Yamamori B., Feng J., Nakano T., Okawa K., Iwamatsu A., Kaibuchi K. Regulation of mysoin phosphatase by rho and rho-associated kinase (Rho-kinase). Science 1996, 273:245-248.
66. Kolodney M.S., Elson E.L. Correlation of myosin light chain phosphorylation with isometric contraction of fibroblasts. J.Biol. Chem. 1993, 268:23850-23855.
67. Kolodney M.S., Wysolmerski R.B. Isometric contraction by fibroblasts and endothelial cells in tissue culture: a quantitative study. J.Cell. Biol. 1992, 117:73-82.
68. Krieg M., Arboleda-Estudillo Y., Puech P.-H., Kafer J., Graner F., Muller D.J., Heisenberg C.-P. Tensile forces govern germ-layer organization in zebrafish. Nat. Cell. Biol. 2008, 10:429-436.
69. Kriparamanan R., Aswath P., Zhou A., Tang L., Nguyen K.T. Nanotopography: cellular responses to nanostructured materials. J.Nanosci. Nanotechnol. 2006, 6:1905-1919.
70. Kshitiz, Park J., Kim P., Helen W., Engler A.J., Levchenko A., Kim D.H. Control of stem cell fate and function by engineering physical microenvironments. Integr. Biol. (Camb.) 2012, 4:1008-1018.
71. Lakshman N., Kim A., Petroll W.M. Characterization of corneal keratocyte morphology and mechanical activity within 3-D collagen matrices. Exp. Eye Res. 2010, 90:350-359.
72. Lakshman N., Petroll W.M. Growth factor regulation of corneal keratocyte mechanical phenotypes in 3-D collagen matrices. Invest. Ophthalmol. Vis. Sci. 2012, 53:1077-1086.
73. Liu C., Feng P., Li X., Song J., Chen W. Expression of MMP-2, MT1-MMP, and TIMP-2 by cultured rabbit corneal fibroblasts under mechanical stretch. Exp. Biol. Med. (Maywood) 2014, 239:907-912.
74. Liu M., Tanswell A.K., Post M. Mechanical force-induced signal transduction in lung cells. Am. J. Physiol. 1999, 277:L667-L683.
75. Lo C.M., Wang H.B., Dembo M., Wang Y.L. Cell movement is guided by the rigidity of the substrate. Biophys. J. 2000, 79:144-152.
76. Meyer-ter-Vehn T., Han H., Grehn F., Schlunck G. Extracellular matrix elasticity modulates TGF-β-induced p38 activation and myofibroblast transdifferentiation in human tenon fibroblasts. Invest. Ophthalmol. Vis. Sci. 2011, 52:9149-9155.
77. Miron-Mendoza M., Seemann J., Grinnell F. The differential regulation of cell motile activity through matrix stiffness and porosity in three dimensional collagen matrices. Biomaterials 2010, 31:6425-6435.
78. Moller-Pedersen T., Cavanagh H.D., Petroll W.M., Jester J.V. Corneal haze development after PRK is regulated by volume of stromal tissue removal. Cornea 1998, 17:627-639.
79. Moller-Pedersen T., Cavanagh H.D., Petroll W.M., Jester J.V. Stromal wound healing explains refractive instability and haze development after photorefractive keratectomy: a 1-year confocal microscopic study. Ophthalmology 2000, 107:1235-1245.
80. Moller-Pedersen T., Li H., Petroll W.M., Cavanagh H.D., Jester J.V. Confocal microscopic characterization of wound repair after photorefractive keratectomy using invivo confocal microscopy. Invest. Ophthalmol. Vis. Sci. 1998, 39:487-501.
81. Moller-Pedersen T., Vogel M., Li H.F., Petroll W.M., Cavanagh H.D., Jester J.V. Quantification of stromal thinning, epithelial thickness, and corneal haze after photorefractive keratectomy using invivo confocal microscopy. Ophthalmology 1997, 104:360-368.
82. Morishige N., Wahlert A.J., Kenney M.C., Brown D.J., Kawamoto K., Chikama T., Nishida T., Jester J.V. Second-harmonic imaging microscopy of normal human and keratoconus cornea. Invest. Ophthalmol. Vis. Sci. 2007, 48:1087-1094.
83. Mudera V.C., Pleass R., Eastwood M., Tarnuzzer R., Schultz G., Khaw P., McGrouther D.A., Brown R.A. Molecular responses of human dermal fibroblasts to dual cues: contact guidance and mechanical load. Cell. Motil. Cytoskel. 2000, 45:1-9.
84. Myrna K.E., Mendonsa R., Russell P., Pot S.A., Liliensiek S.J., Jester J.V., Nealey P.F., Brown D., Murphy C.J. Substratum topography modulates corneal fibroblast to myofibroblast transformation. Invest Ophthalmol. Vis. Sci. 2012, 53:811-816.
85. Netto M.V., Mohan R.R., Ambrosio R., Hutcheon A.E., Zieske J.D., Wilson S.E. Wound healing in the cornea: a review of refractive surgery complications and new prospects for therapy. Cornea 2005, 24:509-522.
86. Parizi M., Howard E.W., Tomasek J.J. Regulation of LPA-promoted myofibroblast contraction: role of rho, myosin light chain kinase, and myosin light chain phosphatase. Exp. Cell. Res. 2000, 254:210-220.
87. Pelham R.J., Wang Y.L. Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc. Natl. Acad. Sci. USA 1997, 94:13661-13665.
88. Pepose J.S., Ubels J.L. The cornea. Adler's Physiology of the Eye 1992, 29-70. Mosby Year Book, St. Louis. W.M. Hart (Ed.).
89. Petroll W.M., Cavanagh H.D., Jester J.V. Dynamic three-dimensional visualization of collagen matrix remodeling and cytoskeletal organization in living corneal fibroblasts. Scanning 2004, 26:1-10.
90. Petroll W.M., Ma L. Localized application of mechanical and biochemical stimuli in 3-D culture. Dev. Dyn. 2008, 237:2726-2736.
91. Petroll W.M., Ma L., Kim A., Ly L., Vishwanath M. Dynamic assessment of fibroblast mechanical activity during Rac-induced cell spreading in 3-D culture. J.Cell. Physiol. 2008, 217:162-171.
92. Petroll W.M., Ma L., Ly L., Vishwanath M. Analysis of the pattern of sub-cellular force generation by corneal fibroblasts following Rho activation. Eye Contact Lens 2008, 34:65-70.
93. Petroll W.M., New K., Sachdev M., Cavanagh H.D., Jester J.V. Radial keratotomy III. Relationship between wound gape and corneal curvature in primate eyes. Invest. Ophthalmol. Vis. Sci. 1992, 33:3283-3291.
94. Petroll W.M., Vishwanath M., Ma L. Corneal fibroblasts respond rapidly to changes in local mechanical stress. Invest. Ophthalmol. Vis. Sci. 2004, 45:3466-3474.
95. Rayan G.M., Parizi M., Tomasek J.J. Pharmacologic regulation of Dupuytren's fibroblast contraction invitro. J.Hand Surg. Br. 1996, 21:1065-1070.
96. Reilly G.C., Engler A.J. Intrinsic extracellular matrix properties regulate stem cell differentiation. J.Biomech. 2010, 43:55-62.
97. Ren R., Hutcheon A.E.K., Guo X.Q., Saeidi N., Melotti S.A., Ruberti J.W., Zieske J.D., Trinkaus-Randall V. Human primary corneal fibroblasts synthesize and deposit proteoglycans in long-term cultures. Dev. Dyn. 2008, 237:2705-2715.
98. Rottner K., Hall A., Small J.V. Interplay between Rac and Rho in the control of substrate contact dynamics. Curr. Biol. 1999, 9:640-648.
99. Roy P., Petroll W.M., Cavanagh H.D., Jester J.V. Exertion of tractional force requires the coordinated upregulation of cell contractility and adhesion. Cell. Motil. Cytoskel. 1999, 43:23-34.
100. Ruberti J.W., Roy A.S., Roberts C.J. Corneal biomechanics and biomaterials. Annu Rev. Biomed. Eng. 2011, 13:269-295.
101. Sadoshima J., Izumo S. The cellular and molecular response of cardiac myocytes to mechanical stress. Annu Rev. Physiol. 1997, 59:551-571.
102. Saeidi N., Guo X., Hutcheon A.E., Sander E.A., Bale S.S., Melotti S.A., Zieske J.D., Trinkaus-Randall V., Ruberti J.W. Disorganized collagen scaffold interferes with fibroblast mediated deposition of organized extracellular matrix invitro. Biotechnol. Bioeng. 2012, 109:2683-2698.
103. Sander E.E., ten Klooster J.P., van Delft S., van der Kammen R.A., Collard J.G. Rac downregulates Rho activity: reciprocal balance between both GTPases determines cellular morphology and migratory behavior. J.Cell. Biol. 1999, 147:1009-1021.
104. Sanderson P.L., Morris A.M., Stanley J.K., Fahmy N.R.M. Lipids and Dupuytren's disease. J.Bone Jt. Surg. 1992, 74B:723-927.
105. Shyy J.Y.-J., Chien S. Role of integrins in endothelial mechanosensing of shear stress. Circ. Res. 2002, 91:769-775.
106. Stepp M.A., Zieske J.D., Trinkaus-Randall V., Kyne B.M., Pal-Ghosh S., Tadvalkar G., Pajoohesh-Ganji A. Wounding the cornea to learn how it heals. Exp. Eye Res. 2014, 121:178-193.
107. Stopak D., Harris A.K. Connective tissue morphogenesis by fibroblast traction. I. Tissue culture observations. Dev. Biol. 1982, 90:383-398.
108. Stopak D., Wessels N.K., Harris A.K. Morphogenetic rearrangement of injected collagen in developing chicken limb buds. Proc. Nat. Acad. Sci. USA 1985, 82:2804-2808.
109. Stramer B.M., Zieske J.D., Jung J.-C., Austin J.S., Fini M.E. Molecular mechanisms controlling the fibrotic repair phenotype in cornea: implications for surgical outcomes. Invest. Ophthalmol. Vis. Sci. 2003, 44:4237-4246.
110. Svitkina T.M., Borisy G.G. Arp2/3 complex and actin depolymerizing factor/cofilin in dendritic organization and treadmilling of actin filament array in lamellipodia. J.Cell. Biol. 1999, 145:1009-1026.
111. Takakuda K., Miyairi H. Tensile behavior of fibroblasts cultured in collagen gel. Biomaterials 1996, 17:1393-1397.
112. Teixeira A.I., Abrams G.A., Bertics P.J., Murphy C.J., Nealey P.F. Epithelial contact guidance on well-defined micro- and nanostructured substrates. J.Cell. Sci. 2003, 116:1881-1892.
113. Teixeira A.I., Nealey P.F., Murphy C.J. Responses of human keratocytes to micro- and nanostructured substrates. J.Biomed. Mater. Res. A 2004, 71A:369-376.
114. Tomasek J.J., Hay E.D., Fujiwara K. Collagen modulates cell shape and cytoskeleton of embryonic corneal and fibroma fibroblasts: distribution of actin, α-actinin and myosin. Dev. Biol. 1982, 92:107-122.
115. Tomasek J.J., McConathy W.J., Checovich W.J., Mosher D.F. Lipoproteins promote fibroblast-mediated collagen lattice contraction. Mol. Biol. Cell. 1992, 3:234A.
116. Totsukawa G., Yamakita Y., Yamashiro S., Hartshorne D.J., Sasaki Y. Distinct roles of ROCK (Rho-kinase) and MLCK in spatial regulation of MLC phosphorylation for assembly of stress fibers and focal adhesions in 3T3 fibroblasts. J.Cell. Biol. 2000, 150:797-806.
117. Tummina S.J., Mitton K.P., Arora J., Zelenka P., Epstein D.L., Russell P. Mechanical stretch alters the actin cytoskeletal network and signal transduction in human trabecular meshwork cells. Invest. Ophthalmol. Vis. Sci. 1998, 39:1361-1371.
118. van Bockxmeer F.M., Martin C.E., Constable I.J. Effect of cyclic AMP on cellular contractility and DNA synthesis in chorioretinal fibroblasts maintained in collagen matrices. Exp. Cell. Res. 1984, 155:413-421.
119. Vishwanath M., Ma L., Jester J.V., Otey C.A., Petroll W.M. Modulation of corneal fibroblast contractility within fibrillar collagen matrices. Invest. Ophthalmol. Vis. Sci. 2003, 44:4724-4735.
120. Wakatsuki T., Elson E.L. Reciprocal interactions between cells and extracellular matrix during remodeling of tissue constructs. Biophys. Chem. 2003, 100:593-605.
121. Wang J., Liu X., Zhong Y. Rho/Rho-associated kinase pathway in glaucoma (Review). Int. J. Oncol. 2013, 43:1357-1367.
122. Wilson S.E. Corneal myofibroblast biology and pathobiology: generation, persistence, and transparency. Exp. Eye Res. 2012, 99:78-88.
123. Wilson S.E., Mohan R.R., Mohan R.R., Ambrosio R., Hong J.W., Lee J.S. The corneal wound healing response: cytokine-mediated interaction of the epithelium, stroma, and inflammatory cells. Prog. Retin Eye Res. 2001, 20:625-637.
124. Winkler M., Chai D., Kriling S., Nien C.J., Brown D.J., Jester B., Juhasz T., Jester J.V. Nonlinear optical macroscopic assessment of 3-D corneal collagen organization and axial biomechanics. Invest. Ophthalmol. Vis. Sci. 2011, 52:8818-8827.
125. Wu J., Du Y., Mann M.M., Yang E., Funderburgh J.L., Wagner W.R. Bioengineering organized, multilamellar human corneal stromal tissue by growth factor supplementation on highly aligned synthetic substrates. Tissue Eng. Part A 2013, 19:2063-2075.
126. Wu J., Du Y., Watkins S.C., Funderburgh J.L., Wagner W.R. The engineering of organized human corneal tissue through the spatial guidance of corneal stromal stem cells. Biomaterials 2012, 33:1343-1352.
127. Yamamoto M., Quantock A.J., Young R.D., Okumura N., Ueno M., Sakamoto Y., Kinoshita S., Koizumi N. Aselective inhibitor of the Rho kinase pathway, Y-27632, and its influence on wound healing in the corneal stroma. Mol. Vis. 2012, 18:1727-1739.
128. Yeung T., Georges P.C., Flanagan L.A., Marg B., Ortiz M., Funaki M., Zahir N., Ming W., Weaver V., Janmey P.A. Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion. Cell. Motil. Cytoskel. 2005, 60:24-34.
129. Zhou C. The Functional Roles of Rho-kinase and Matrix Metalloproteinases in Regulating Corneal Stromal Cell Mechanics in 3-D Collagen Matrices 2014, Biomedical Engineering Program. University of Texas Southwestern Medical Center.
130. Zhou C., Petroll W.M. Rho kinase regulation of fibroblast migratory mechanics in fibrillar collagen matrices. Cell. Mol. Bioeng. 2010, 3:76-83.
131. Zhou C., Petroll W.M. MMP regulation of corneal keratocyte motility and mechanics in 3-D collagen matrices. Exp. Eye Res. 2014, 121:147-160.