Epidermal growth factor synergism with TGF-β1 via PI-3 kinase activity in corneal keratocyte differentiation

Investigative Ophthalmology and Visual Science

Volumn 49, Issue 7, 2008, Pages 2936-2945

  He, Jiucheng ^a   Bazan, Haydee E P ^a  

^a LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE DEHYDROGENASE; ALPHA SMOOTH MUSCLE ACTIN; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE INHIBITOR; KI 67 ANTIGEN; NEUTRALIZING ANTIBODY; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; TRANSFORMING GROWTH FACTOR BETA1; RECOMBINANT PROTEIN;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CELL STIMULATION; COMPUTER PROGRAM; CONTROLLED STUDY; CORNEA CELL; CULTURE MEDIUM; DENDRITIC CELL; DIAGNOSTIC IMAGING; ENZYME ACTIVITY; ENZYME INHIBITION; EXTRACELLULAR MATRIX; IMMUNOCYTOCHEMISTRY; MICROSCOPE; MYOFIBROBLAST; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RABBIT; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANIMAL; CELL CULTURE; CELL MOTION; CORNEA; CYTOLOGY; DRUG EFFECT; DRUG POTENTIATION; ENZYMOLOGY; FIBROBLAST; HUMAN; METABOLISM; PHYSIOLOGY; SMOOTH MUSCLE FIBER;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; CELL DIFFERENTIATION; CELL MOVEMENT; CELLS, CULTURED; CORNEA; DRUG SYNERGISM; EPIDERMAL GROWTH FACTOR; FIBROBLASTS; HUMANS; MYOCYTES, SMOOTH MUSCLE; RABBITS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA1;

EID: 48249153039     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.07-0900     Document Type: Article

References (66)

1. Nishida T, Yasumoto K, Otori T, Desaki J. The network structure of corneal fibroblasts in the rat as revealed by scanning electron microscopy. Invest Ophthalmol Vis Sci. 1988;29:1887-1890. (Pubitemid 19015079)
2. Poole CA, Brookes NH, Clover GM. Keratocyte networks visualized in the living cornea using vital dyes. J Cell Sci. 1993;106:685-692. (Pubitemid 223000934)
3. Jester JV, Barry PA, Lind GL, Petroll WM, Garana R, Cavanagh HD. Corneal keratocytes: in situ and in vitro organization of cytoskeletal contractile proteins. Invest Ophthalmol Vis Sci. 1994;35:730-735. (Pubitemid 24078133)
4. Jalbert I, Stapleton F, Papas E, Sweeney DF, Coroneo M. In vivo confocal microscopy of the human cornea. Br J Ophthalmol. 2003;87:225-236. (Pubitemid 36152753)
5. Davison PF, Galbavy EJ. Connective tissue remodeling in corneal and scleral wounds. Invest Ophthalmol Vis Sci. 1986;27:1478-1484. (Pubitemid 16004396)
6. Jester JV, Petroll WM, Cavanagh HD. Corneal stromal wound healing in refractive surgery: the role of myofibroblasts. Prog Retin Eye Res. 1999;18:311-356. (Pubitemid 29092610)
7. Fini ME. Keratocyte and fibroblast phenotypes in the repairing cornea. Prog Retin Eye Res. 1999;18:529-551. (Pubitemid 29126966)
8. Cintron C, Hassinger LC, Kublin CL, Cannon DJ. Biochemical and ultrastructural changes in collagen during corneal wound healing. J Ultrastruct Res. 1978;65:13-22. (Pubitemid 9074157)
9. Garana RMR, Petroll WM, Chen WT, et al. Radial keratotomy, II: role of the myofibroblast in corneal wound contraction. Invest Ophthalmol Vis Sci. 1992;33:3271-3282.
10. Bazan HEP. Cellular and molecular events in corneal wound healing: significance of lipid signaling. Exp Eye Res. 2005;4:453-463. (Pubitemid 40387514)
11. Ottino P, He J, Axelrad TW, Bazan HEP. PAF-induced furin and MT1-MMP expression is independent of MMP-2 activation in corneal myofibroblasts. Invest Ophthalmol Vis Sci. 2005;46:487-496. (Pubitemid 40270326)
12. Esquenazi S, He J, Bazan NG, Bazan HEP. Comparison of corneal wound healing response in photorefractive keratectomy and laser-assisted subepithelial keratectomy. J Caract Refract Surg. 2005; 31:1632-1639. (Pubitemid 41208046)
13. He J, Bazan NG, Bazan HEP. Alkali-induced corneal stromal melting prevention by a novel platelet-activating factor (PAF) receptor antagonist. Arch Ophthalmol. 2006;124:70-78. (Pubitemid 43063891)
14. He J, Bazan HEP. Synergistic effect of platelet-activating factor and tumor necrosis factor-α on corneal myofibroblast apoptosis. Invest Ophthalmol Vis Sci. 2006;47:883-891. (Pubitemid 46768318)
15. Zhang K, Rekhter MD, Gordon D, Phan SH. Myofibroblasts and their role in lung collagen gene expression during pulmonary fibrosis: a combined immunohistochemical and in situ hybridization study. Am J Pathol. 1994;145:114-125. (Pubitemid 24217490)
16. Bazan HEP, Ottino P. The role of platelet-activating factor in the corneal response to injury. Prog Ret Eye Res. 2002;21:449-464. (Pubitemid 35245966)
17. Imanishi J, Kamiyama K, Iguichi I, Kita M, Sotozono C, Kinoshita S. Growth factors: importance in wound healing and maintenance of transparency of the cornea. Prog Retin Eye Res. 2000;19:113-129.
18. Wilson SE. Analysis of the keratocyte apoptosis, keratocyte proliferation, and myofibroblast transformation responses after photorefractive keratectomy and laser in situ keratomileusis. Trans Am Ophthalmol Soc. 2002;100:411-433. (Pubitemid 37039381)
19. Esquenazi S, He J, Bazan HE, Bazan NG. Prevention of experimental diffuse lamellar keratitis using a novel platelet-activating factor receptor antagonist. J Cataract Refract Surg. 2004;30:884-891. (Pubitemid 38501486)
20. Funderburg JL, Funderburg ML, Mann M, Corpuz L, Roth MR. Proteoglycan expression during transforming growth factor beta-induced keratocyte- myofibroblast transdifferentiation. J Biol Chem. 2001;276:44173-44178. (Pubitemid 37383990)
21. 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. (Pubitemid 32954853)
22. Jester JV, Ho-Chang J. 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. (Pubitemid 37188733)
23. Musselmann K, Alexandrou B, Kane B, Hassell JR. Maintenance of the keratocyte phenotype during cell proliferation stimulated by insulin. J Biol Chem. 2005;280:32634-32639. (Pubitemid 41368306)
24. Jester JV, Barry-Lane PA, Cavanagh HD, Petroll WM. Induction of alpha-smooth muscle actin expression and myofibroblast transformation in cultured corneal keratocytes. Cornea. 1996;15:505-516. (Pubitemid 26271790)
25. Jorisson RN, Walker F, Pouliot N, Garrett TPJ, Ward CW, Burgess AW. Epidermal growth factor receptor: mechanisms of activation and signaling. Exp Cell Res. 2003;284:31-53. (Pubitemid 36331965)
26. Nishida T, Tanaka H, Nakagawa S, Sasabe T, Awata T, Manabe R. Fibronectin synthesis by the rabbit cornea: effect of mouse epidermal growth factor and cyclic AMP analogs. Jpn J Ophthalmol. 1984;28:196-202. (Pubitemid 14122850)
27. Wilson SE, He Y-G, Lioyd SA. EGF, EGF receptor, basic FGF, TGF beta-1, and IL-1 alpha mRNA in human corneal epithelial cells and stromal fibroblasts. Invest Ophthalmol Vis Sci. 1992;32:1756-1765.
28. Nakamura Y, Sotozono C, Kinoshita S. The epidermal growth factor receptors (EGFR): role in corneal wound healing and homeostasis. Exp Eye Res. 2001;72:511-517. (Pubitemid 32977221)
29. Kitazawa T, Kinoshita S, Fujita K, et al. The mechanism of accelerated corneal epithelial healing by human epidermal growth factor. Invest Ophthalmol Vis Sci. 1990;31:1773-1778. (Pubitemid 20350901)
30. Hongo M, Itoi M, Yamaguchi N, Imanishi J. Distribution of epidermal growth factor (EGF) receptors in rabbit corneal epithelial cells, keratocytes, and endothelial cells, and the changes induced by transforming growth factor-β1. Exp Eye Res. 1992;54:9-16.
31. Maldonado BA, Furcht LT. Epidermal growth factor stimulates integrin-mediated cell migration of cultured human corneal epithelial cells on fibronectin and arginine-glycine-aspartic acid peptide. Invest Ophthalmol Vis Sci. 1995;36:2120-2126.
32. Zieske JD, Takahashi H, Hutcheon AEK, Dabbone AG. Activation of epidermal growth factor receptor during corneal epithelial migration. Invest Ophthalmol Vis Sci. 2000;41:1346-1355. (Pubitemid 30261856)
33. Brightwell JR, Riddle SL, Eiferman RA, et al. Biosynthetic human EGF accelerates healing on neodecadron-treated primate corneas. Invest Ophthalmol Vis Sci. 1985;26:105-110. (Pubitemid 15163619)
34. Woost PG, Brightwell J, Eiferman RA, Schultz GS. Effect of growth factors with dexamethasone on healing of rabbit corneal stromal incisions. Exp Eye Res. 1985;40:47-60. (Pubitemid 15133242)
35. Petroutsos G, Sebag J, Courtois Y. Epidermal growth factor increases tensile strength during wound healing. Ophthalmic Res. 1986;18:299-300. (Pubitemid 17170458)
36. Mathers WD, Sherman M, Fryczkowski A, Jester JV. Dose-dependent effects of epidermal growth factor on corneal wound healing. Invest Ophthalmol Vis Sci. 1989;30:2403-2406. (Pubitemid 20004242)
37. Leibowitz HM, Morrello S Jr, Stern M, Kupferman A. Effect of topically administered epidermal growth factor on corneal wound strength. Arch Ophthalmol. 1990;108:734-737. (Pubitemid 20168837)
38. Brazzell RK, Stern ME, Aquavella JV, Beuerman RW, Baird L. Human recombinant epidermal growth factor in experimental corneal wound healing. Invest Ophthalmol Vis Sci. 1991;32:336-340.
39. Beaubien J, Boisjoly HM, Gagnon P, Guidoin R. Mechanical properties of the rabbit cornea during wound healing after treatment with epidermal growth factor. Can J Ophthalmol. 1994;29:61-65. (Pubitemid 24190185)
40. Masur SK, Dewall HS, Dinh TT, Erenburg I, Petridou S. Myofibroblasts differentiate from fibroblasts when plated at low density. Proc Natl Acad Sci U S A. 1996;93:4219-4223. (Pubitemid 26144266)
41. Tomasek JJ, Gabbiani G, Hinz B, Chaponnier C, Brown RA. Myofibroblasts and mechano-regulation of connective tissue remodeling. Nat Rev Mol Cell Biol. 2002;3:349-363. (Pubitemid 34619269)
42. Suda T, Nishida T, Ohashi Y, Nakagawa S, Manabe R. Fibronectin appears at the site of corneal stromal wound in rabbits. Curr Eye Res. 1981;1:553-556.
43. Anderson JA, Binder PS, Rock ME, et al. Human excimer laser keratectomy: immunohistochemical analysis of healing. Arch Ophthalmol. 1994;114:54-60.
44. Latvala T, Tervo K, Mustonen R, et al. Expression of cellular fibronectin and tenascin in the rabbit cornea after excimer laser photorefractive keratectomy: a 12-month study. Br J Ophthalmol. 1995;79:65-69.
45. Armstrong DJ, Hiscott P, Batterbury M, Kaye S. Corneal stromal cells (keratocytes) express thrombospondins 2 and 3 in wound repair phenotype. Int J Biochem Cell Biol. 2002;34:588-593. (Pubitemid 34270711)
46. Yu JT, Foster RG, Dean DC. Transcriptional repression by Rb-E2F and regulation of anchorage-independent survival. Mol Cell Biol. 2001;21:3325-3335. (Pubitemid 32381768)
47. Arciniegas E, Sutton AB, Allen TD, Shor AM. Transforming growth factor beta 1 promotes the differentiation of endothelial cells into smooth muscle-like cells in vitro. J Cell Sci. 1992;103:521-529.
48. Ronnov-Jessen L, Petersen OW. Induction of alpha-smooth muscle actin by transforming growth factor-beta1 in quiescent human breast gland fibroblasts. Lab Invest. 1993;68:696-707. (Pubitemid 23202798)
49. Verbeek MM, Otte-Holler I, Wesseling P, Ruiter DJ, de Waal RM. Induction of alpha-smooth muscle actin expression in cultured human brain pericytes by transforming growth factor-beta 1. Am J Pathol. 1994;144:372-382. (Pubitemid 2041437)
50. Hales AM, Schulz MW, Chamberlain CG, McAvoy JW. TGF-beta 1 induces lens cells to accumulate alpha-smooth muscle actin, a marker for subcapsular cataracts. Curr Eye Res. 1994;13:885-890.
51. Funderburgh JL, Mann MM, Funderburgh ML. Keratocyte phenotype mediates proteoglycan structure: a role for fibroblasts in corneal fibrosis. J Biol Chem. 2003;278:45629-45637. (Pubitemid 37432705)
52. Goldkorn T, Mendelsohn J. Transforming growth factor beta modulates phosphorylation of the epidermal growth factor receptor and proliferation of A431 cells. Cell Growth Differ. 1992;3:101-109.
53. Bendell JJ, Dorrington JH. Epidermal growth factor influences growth and differentiation of rat granulosa cells. Endocrinology. 1990;127:533-540. (Pubitemid 20248089)
54. Thompson KL, Assoian R, Rosner MR. Transforming growth factor-beta increases transcription of the genes encoding the epidermal growth factor receptor and fibronectin in normal rat kidney fibroblasts. J Biol Chem. 1988;263:19519-19524. (Pubitemid 19016432)
55. Andresen JL, Ehlers N. Chemotaxis of human keratocytes is increased by platelet-derived growth factor-BB, epidermal growth factor, transforming growth factor-alpha, acidic fibroblast growth factor, insulin-like growth factor-I, and transforming growth factor-beta. Curr Eye Res. 1998;17:79-87. (Pubitemid 28039672)
56. Andresen JL, Ledet T, Ehlers N. Keratocyte migration and peptide growth factors: the effect of PDGF, bFGF, EGF, IGF-I, aFGF and TGF-beta on human keratocyte migration in a collagen gel. Curr Eye Res. 1997;16:605-613. (Pubitemid 27267659)
57. Pancholi S, Tullo A, Khaliq A, Foreman D, Boulton M. The effects of growth factors and conditioned media on the proliferation of human corneal epithelial cells and keratocytes. Graefes Arch Clin Exp Ophthalmol. 1998;236:1-8. (Pubitemid 28080563)
58. Sharma GD, He J, Bazan HEP. P38 and ERK1/2 coordinate cellular migration and proliferation in epithelial wound healing: evidence of cross-talk activation between MAP kinase cascades. J Biol Chem. 2003;278:21989-21997. (Pubitemid 36792607)
59. Enomoto A, Murakami H, Asai N, et al. Akt/PKB regulates actin organization and cell motility via girdin/APE. Dev Cell. 2005;9: 389-402. (Pubitemid 41235808)
60. Galaria II, Nicholl SM, Roztocil E, Davies MG. Urokinase-induced smooth muscle cell migration requires PI3-K and Akt activation. J Surg Res. 2005;127:46-52. (Pubitemid 40814629)
61. Leventhal PS, Shelden EA, Kim B, Feldman EL. Tyrosine phosphorylation of paxillin and focal adhesion kinase during insulin-like growth factor-I-stimulated lamellipodial advance. J Biol Chem. 1997;272:5214-5218. (Pubitemid 27090081)
62. Pankov R, Yamada KM. Fibronectin at a glance. J Cell Sci. 2002; 115:3861-3863. (Pubitemid 35256486)
63. Tervo K, van Setten GB, Beuerman RW, Virtanen I, Tarkkanen A, Tervo T. Expression of tenascin and cellular fibronectin in the rabbit cornea after anterior keratectomy: immunohistochemical study of wound healing dynamics. Invest Ophthalmol Vis Sci. 1991;32:2912-2918.
64. Andresen JL, Ledet T, Hager H, Josephen K, Ehlers N. The influence of corneal stromal matrix proteins on the migration of corneal fibroblasts. Exp Eye Res. 2000;71:33-43. (Pubitemid 30688305)
65. Taliana L, Evans MD, Dimitrijevich SD, Steele JG. Vitronectin or fibronectin is required for corneal fibroblast-seeded collagen gel contraction. Invest Ophthalmol Vis Sci. 2000;41:103-109. (Pubitemid 30036555)
66. Liu Y, Yanai R, Lu Y, Kimura K, Nishida T. Promotion by fibronectin of collagen gel contraction mediated by human corneal fibroblasts. Exp Eye Res. 2006;83:1196-1204. (Pubitemid 44397040)