Growth factor regulation of corneal keratocyte differentiation and migration in compressed collagen matrices

Investigative Ophthalmology and Visual Science

Volumn 51, Issue 2, 2010, Pages 864-875

  Kim, Areum ^a   Lakshman, Neema ^a   Karamichos, Dimitris ^a   Matthew Petroll, W ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; COLLAGEN; PHALLOIDIN; PLATELET DERIVED GROWTH FACTOR; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA2; ACTIN;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL ELONGATION; CELL MIGRATION; CELL STIMULATION; CELL STRUCTURE; CELL TRANSFORMATION; CELL VIABILITY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CORNEA CELL; CULTURE MEDIUM; EXTRACELLULAR MATRIX; MYOFIBROBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RABBIT; ANIMAL; CELL COUNT; CELL MOTION; CELL SURVIVAL; CORNEA STROMA; CYTOLOGY; DRUG EFFECT; FIBROBLAST; FLUORESCENCE MICROSCOPY; METABOLISM;

ACTINS; ANIMALS; CELL COUNT; CELL DIFFERENTIATION; CELL MOVEMENT; CELL SURVIVAL; COLLAGEN; CORNEAL STROMA; EXTRACELLULAR MATRIX; FIBROBLASTS; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; PLATELET-DERIVED GROWTH FACTOR; RABBITS; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA2;

EID: 77449092443     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.09-4200     Document Type: Article

References (88)

1. Netto MV, Mohan RR, Ambrosio R, Hutcheon AEK, Zieske JD, Wilson SE. Wound healing in the cornea: a review of refractive surgery complications and new prospects for therapy. Cornea. 2005;24:509-522.
2. Jester JV, Barry PA, Lind GJ, Petroll WM, Garana R, Cavanagh HD. Corneal keratocytes: in situ and in vitro organization of cytoskeletal contractile proteins. Invest Ophthalmol Vis Sci. 1994;35:730-743.
3. Jester JV, Petroll WM, Cavanagh HD. Corneal stromal wound healing in refractive surgery: the role of the myofibroblast. Prog Retinal Eye Res. 1999;18:311-356.
4. Stramer BM, Zieske JD, Jung J-C, Austin JS, Fini ME. Molecular mechanisms controlling the fibrotic repair phenotype in cornea: implications for surgical outcomes. Invest Ophthalmol Vis Sci. 2003;44:4237-4246.
5. Petroll WM, New K, Sachdev M, Cavanagh HD, Jester JV. Radial keratotomy, III: relationship between wound gape and corneal curvature in primate eyes. Invest Ophthalmol Vis Sci. 1992;33: 3283-3291.
6. Dupps WJ, Wilson SE. Biomechanics and wound healing in the cornea. Exp Eye Res. 2006;83:709-720.
7. Tuli SS, Liu R, Chen C, Blalock TD, Goldstein M, Schultz GS. Immunohistochemical localization of EGF, TGF-α, TGF-β, and their receptors in rat corneas during healing of excimer laser ablation. Curr Eye Res. 2006;31:709-719.
8. Long CJ, Roth MR, Tasheva ES, Funderburgh M, Smit R, Conrad GW. Fibroblast growth factor-2 promotes keratan sulfate proteoglycan expression by keratocytes in vitro. J Biol Chem. 2000;275: 13918-13923.
9. Beales MP, Funderburgh JL, Jester JV, Hassell JR. Proteoglycan synthesis by bovine keratocytes and corneal fibroblasts: maintenance of the keratocyte phenotype in culture. Invest Ophthalmol Vis Sci. 1999;1658-1663.
10. Dahl IMS. Biosynthesis of proteoglycans and hyaluronate in rabbit corneal fibroblast cultures: variation with age of the cell line and effect of fetal calf serum. Exp Eye Res. 1981;32:419-433.
11. Hassell JR, Schrecengost PK, Rada JA, Sundaraj N, Sosi G, Thoft RA. Biosynthesis of stromal matrix proteoglycans and basement membrane components by human corneal fibroblasts. Invest Ophthalmol Vis Sci. 1992;33:547-557.
12. Blalock TD, Duncan MR, Varela JC, et al. 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. Garrett Q, Khaw PT, Blalock TD, Schultz GS, Grotensdorst GR, Daniels JT. 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.
14. Maltseva O, Folger P, Zekaria D, Petridou S, Masur SK. Fibroblast growth factor reversal of the corneal myofibroblast phenotype. Invest Ophthalmol Vis Sci. 2001;42:2490-2495.
15. Jester JV, Chang J-H. Modulation of cultured corneal keratocyte phenotype by growth factors/cytokines control in vitro contractility and extracellular matrix contraction. Exp Eye Res. 2003;77: 581-592.
16. Jester JV, Huang J, Barry-Lane PA, Kao WW, Petroll WM, Cavanagh HD. Transforming growth factor(beta)-mediated corneal myofibroblast differentiation requires actin and fibronectin assembly. Invest Ophthalmol Vis Sci. 1999;40:1959-1967.
17. Jester JV, Huang J, Fisher S, et al. Myofibroblast differentiation of normal human keratocytes and hTERT, extended-life, human corneal fibroblasts. Invest Ophthalmol Vis Sci. 2003;44:1850-1858.
18. Jester JV, Huang J, Petroll WM, Cavanagh HD. TGFbeta induced myofibroblast differentiation of rabbit keratocytes requires synergistic TGFbeta, PDGF and integrin signalling. Exp Eye Res. 2002; 75:645-657.
19. He J, Bazan HEP. Epidermal growth factor synergism with TGF-β1 via PI-3 kinase activity in corneal keratocyte differentiation. Invest Ophthalmol Vis Sci. 2008;49:2936-2945.
20. Etheredge L, Kane BP, Hassell JR. The effect of growth factor signaling on keratocytes in vitro and its relationship to the phases of stromal wound repair. Invest Ophthalmol Vis Sci. 2009;50: 3128-3136.
21. Bard JBL, Hay ED. The behavior of fibroblasts from the developing avian cornea: morphology and movement in situ and in vitro. J Cell Biol. 1975;67:400-418.
22. Cukierman E, Pankov R, Yamada KM. Cell interactions with threedimensional matrices. Curr Opin Cell Biol. 2002;14:633-639.
23. Cukierman E, Pankov R, Stevens DR, Yamada KM. Taking cellmatrix adhesions to the third dimension. Science. 2001;294:1708-1712.
24. Doane KJ, Birk DE. Fibroblasts retain their tissue phenotype when grown in three-dimensional collagen gels. Exp Cell Res. 1991;195: 432-442.
25. Friedl P, Brocker E-B. The biology of cell locomotion within threedimensional extracellular matrix. Cell Mol Life Sci. 2000;57:41-64.
26. Tomasek JJ, Hay ED, 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.
27. Abbott A. Biology's new dimension. Nature. 2003;424:870-872.
28. Rhee S, Jiang H, Ho C, Grinnell F. Microtubule function in fibroblast spreading is modulated according to the tension state of cell-matrix interactions. Proc Natl Acad Sci USA. 2007;104:5425-5430.
29. Grinnell F, Ho C-H, Tamariz E, Lee DJ, Skuta G. Dendritic fibroblasts in three-dimensional collagen matrices. Mol Cell Biol. 2003; 14:384-395.
30. Doyle AD, Wang FW, Matsumoto K, Yamada KM. One-dimensional topography underlies three-dimensional fibrillar cell migration. J Cell Biol. 2009;184:481-490.
31. Bell E, Ivarsson B, Merril C. Production of a tissue-like structure by contraction of collagen lattices by human fibroblasts of different proliferative potential in vivo. Proc Natl Acad Sci USA. 1979;76: 1274-1278.
32. Elsdale T, Bard J. Collagen substrata for studies on cell behavior. J Cell Biol. 1972;54:626-637.
33. Grinnell F, Lamke CR. Reorganization of hydrated collagen lattices by human skin fibroblasts. J Cell Sci. 1984;66:51-63.
34. Stopak D, Harris AK. Connective tissue morphogenesis by fibroblast traction. Dev Biol. 1982;90:383-398.
35. Grinnell F. Fibroblast-collagen matrix contraction: growth-factor signalling and mechanical loading. Trends Cell Biol. 2000;10:362-365.
36. Petroll WM, Ma L. Direct, dynamic assessment of cell-matrix interactions inside fibrillar collagen lattices. Cell Motil Cytoskeleton. 2003;55:254-264.
37. Petroll WM, Ma L, Jester JV. Direct correlation of collagen matrix deformation with focal adhesion dynamics in living corneal fibroblasts. J Cell Sci. 2003;116:1481-1491.
38. Vishwanath M, Ma L, Jester JV, Otey CA, Petroll WM. Modulation of corneal fibroblast contractility within fibrillar collagen matrices. Invest Ophthalmol Vis Sci. 2003;44:4724-4735.
39. Kim A, Lakshman N, Petroll WM. Quantitative assessment of local collagen matrix remodeling in 3D culture: the role of Rho kinase. Exp Cell Res. 2006;312:3683-3692.
40. Lakshman N, Kim A, Bayless KJ, Davis GE, Petroll WM. Rho plays a central role in regulating local cell-matrix mechanical interactions in 3D culture. Cell Motil Cytoskeleton. 2007;64:434-445.
41. Petroll WM, Cavanagh HD, Jester JV. Dynamic three-dimensional visualization of collagen matrix remodeling and cytoskeletal organization in living corneal fibroblasts. Scanning. 2004;26:1-10.
42. Doillon DJ, Watsky MA, Hakim M, et al. A collagen-based scaffold for a tissue engineered human cornea: physical and physiological properties. Int J Artif Organs. 2003;26:764-773.
43. Duan X, Sheardown H. Dendrimer cross-linked collagen as a corneal tissue engineering scaffold: mechanical properties and corneal epithelial cell interactions. Biomaterials. 2006;27:4608-4617.
44. Duan X, Sheardown H. Incorporation of cell-adhesion peptides into collagen scaffolds promotes corneal epithelial stratification. J Biomater Sci. 2007;18:701-711.
45. Rafat M, Li F, Fagerholm P, et al. PEG-stabilized carbodiimide crosslinked collagen-chitosan hydrogels for corneal tissue engineering. Biomaterials. 2008;29:3960-3972.
46. Greiling D, Clark RA. Fibronectin provides a conduit for fibroblast transmigration from collagenous stroma into fibrin clot provisional matrix. J Cell Sci. 1997;100:861-870.
47. Zieske JD, Mason VS, Wasson ME, et al. Basement membrane assembly and differentiation of cultured corneal cells: importance of culture environment and endothelial cell interaction. Exp Cell Res. 1994;214:621-633.
48. Minami Y, Sugihara H, Oono S. Reconstruction of cornea in threedimensional collagen gel matrix culture. Invest Ophthalmol Vis Sci. 1993;34:2316-2324.
49. Ko J-A, Liu Y, Yanai R, Chikama T, Takezawa T, Nishida T. Upregulation of tight-junction proteins in corneal epithelial cells by corneal fibroblasts in collagen vitrigel cultures. Invest Ophthalmol Vis Sci. 2008;49:113-119.
50. Orwin EJ, Hubel A. In vitro culture characteristics of corneal epithelial, endothelial, and keratocyte cells in a native collagen matrix. Tissue Eng. 2000;6:307-319.
51. Ren R, Hutcheon AEK, Guo XQ, et al. Human primary corneal fibroblasts synthesize and deposit proteoglycans in long-term cultures. Dev Dyn. 2008;237:2705-2715.
52. Guo XQ, Hutcheon AE, Melotti SA, Zieske JD, Trinkaus-Randall V, Ruberti JW. Morphologic characterization of organized extracellular matrix deposition by ascorbic acid-stimulated human corneal fibroblasts. Invest Ophthalmol Vis Sci. 2007;48:4056-4060.
53. Brown RA, Wiseman M, Chuo C-B, Cheema U, Nazhat SN. Ultrarapid engineering of biomimetic materials and tissues: fabrication of nano-and microstructures by plastic compression. Adv Funct Mater. 2005;15:1762-1770.
54. Bitar M, Salih V, Brown RA, Nazhat SN. Effect of multiple unconfined compression on cellular dense collagen scaffolds for bone tissue engineering. J Mater Sci: Mater Med. 2007;18: 237-244.
55. Bitar M, Brown RA, Salih V, Asmeret GK, Knowles JC, Nazhat SN. Effect of cell density on osteoblastic differentiation and matrix degradation of biomimetic dense collagen scaffolds. Biomacromolecules. 2008;9:129-135.
56. Eastwood M, Mudera VC, McGrouther DA, Brown RA. Effect of precise mechanical loading on fibroblast populated collagen lattices: morphological changes. Cell Motil Cytoskeleton. 1998;40: 13-21.
57. Mudera VC, Pleass R, Eastwood M, et al. Molecular responses of human dermal fibroblasts to dual cues: contact guidance and mechanical load. Cell Motil Cytoskeleton. 2000;45:1-9.
58. Neel EAA, Cheema U, Knowles JC, Brown RA, Nazhat SN. Use of multiple unconfined compression for control of collagen gel scaffold density and mechanical properties. Soft Matter. 2006;2:986-992.
59. Petroll WM, Ma L, Kim A, Ly L, Vishwanath M. Dynamic assessment of fibroblast mechanical activity during Rac-induced cell spreading in 3D culture. J Cell Physiol. 2008;217:162-171.
60. Jester JV, Petroll WM, Barry PA, Cavanagh HD. Expression of α-smooth muscle (α-SM) actin during corneal stromal wound healing. Invest Ophthalmol Vis Sci. 1995;36:809-819.
61. Karamichos D, Lakshman N, Petroll W. An experimental model for assessing fibroblasts migration in 3D collagen matrices. Cell Motil Cytoskeleton. 2009;66:1-9.
62. Grinnell F, Rocha LB, 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.
63. Friedl P, Noble PB, Zanker KS. T lymphocyte locomotion in a three-dimensional collagen matrix. J Immunol. 1995;154:4973-4985.
64. Friedl P, Maaser K, Klein CE, Niggemann B, Krohne G, Zanker KS. Migration of highly aggressive MV3 melanoma cells in 3Dimensional collagen lattices results in local matrix reorganization and shedding of alpha2 and beta1 integrins and CD44. Cancer Res. 1997;57:2061-2070.
65. Tuominen ISJ, Tervo TMT, Teppo A-M, Valle TU, Gronhagen-Riska C, Vesaluoma MH. Human tear fluid PDGF-BB, TNF-α and TGF-β1 vs corneal haze and regeneration of corneal epithelium and subbasal nerve plexus after PRK. Exp Eye Res. 2001;72:631-641.
66. West-Mays J, Dwivedi D. The keratocyte: corneal stromal cell with variable repair pheonotypes. Int J Biochem Cell Biol. 2006;38: 1625-1631.
67. Funderburgh J, Funderburgh M, Mann M, Corpuz L, Roth M. Proteoglycan expression during transforming growth factor betainduced keratocyte-myofibroblast transdifferentiation. J Biol Chem. 2001;276:44173-44178.
68. Sabeth F, Ota I, Holmbeck K, et al. Tumor cell traffic through the extracellular matrix is controlled by the membrane-anchored collagenase MTI-MMP. J Cell Biol. 2004;167:769-781.
69. Lauffenburger DA, Horwitz AF. Cell migration: a physically integrated molecular process (review). Cell. 1996;84:359-369.
70. Raftopoulou M, Hall A. Cell migration: Rho GTPases lead the way. Dev Biol. 2004;265:23-32.
71. Andresen JL, 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.
72. 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;107:3643-3564.
73. Craig SW, Johnson RP. Assembly of focal adhesions: progress, paradigms, and portents. Curr Opin Cell Biol. 1996;8:74-85.
74. Kolodney MS, Elson EL. Correlation of myosin light chain phosphorylation with isometric contraction of fibroblasts. J Biol Chem. 1993;268:23850-23855.
75. Tomasek JJ, McConathy WJ, Checovich WJ, Mosher DF. Lipoproteins promote fibroblast-mediated collagen lattice contraction. Mol Biol Cell. 1992;3:234A.
76. Parizi M, Howard EW, Tomasek JJ. Regulation of LPA-promoted myofibroblast contraction: role of rho, myosin light chain kinase, and myosin light chain phosphotase. Exp Cell Res. 2000;254:210-220.
77. Tamariz E, Grinnel F. Modulation of fibroblast morphology and adhesion during collagen matrix remodeling. Mol Biol Cell. 2002; 13:3915-3929.
78. Jiang H, Rhee S, Ho C-H, Grinnell F. Distinguishing fibroblast promigratory and procontractile growth factor environments in 3D collagen matrices. FASEB J. 2008;22:2151-2160.
79. Petroll WM, 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.
80. Anderson S, DiCesare L, Tan I, Leung T, SundarRaj N. Rhomediated assembly of stress fibers is differentially regulated in corneal fibroblasts and myofibroblasts. Exp Cell Res. 2004;298:574-583.
81. Xing D, Bonanno JA. Effect of cAMP on TGFbeta-1 induced corneal keratocyte-myofibroblast transformation. Invest Ophthalmol Vis Sci. 2009;50:626-633.
82. Tomasek JJ, Vaughan MB, Kropp BP, et al. Contraction of myofibroblasts in granulation tissue is dependent on Rho/Rho kinase, myosin light chain phosphatase activity. Wound Repair Regen. 2006;14:313-320.
83. Prass M, Jacobson K, Mogilner A, Radmacher M. Direct measurement of the lamellipodial protrusive force in a migrating cell. J Cell Biol. 2006;174:767-772.
84. Abraham VC, Krishnamurthi V, Taylor DL, Lanni F. The actin-based nanomachine at the leading edge of migrating cells. Biophys J. 1999;77:1721-1732.
85. Bohnet S, Ananthakrishnan R, Mogilner A, Meister J-J, Verkhovsky AB. Weak force stalls protrusion at the leading edge of the lamellipodium. Biophys J. 2006;90:1810-1820.
86. Marcy Y, Prost J, Carlier M-F, Sykes C. Forces generated during actin-based propulsion: a direct measurement by micromanipulation. Proc Natl Acad Sci U S A. 2004;101:5992-5997.
87. Pollard TD, Borisy GG. Cellular motility driven by assembly and disassembly of actin filaments. Cell. 2003;112:453-465.
88. Petroll WM, Ma L. Localized application of mechanical and biochemical stimuli in 3D culture. Dev Dynamics. 2008;237:2726-2736.