Induction of corneal myofibroblasts by lens-derived transforming growth factor β1 (TGFβ1): A transgenic mouse model

Brain Research Bulletin

Volumn 81, Issue 2-3, 2010, Pages 287-296

  Reneker, Lixing W ^a   Bloch, Amy ^a   Xie, Leike ^a   Overbeek, Paul A ^b   Ash, John D ^c  

^a University of Missouri   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

Author keywords

Cornea; EMT; Mouse and eye; TGF ; Wound healing

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CADHERIN; CADHERIN 11; MOLECULAR MARKER; NERVE CELL ADHESION MOLECULE; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA2; UNCLASSIFIED DRUG; UVOMORULIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASEMENT MEMBRANE; CELL COMMUNICATION; CELL CONTACT; CELLULAR, SUBCELLULAR AND MOLECULAR BIOLOGICAL PHENOMENA AND FUNCTIONS; CONTROLLED STUDY; CORNEA CELL; CORNEA DISEASE; CORNEA ENDOTHELIUM; CORNEA EPITHELIUM; CORNEA STROMA; DOWN REGULATION; ENDOTHELIAL TO MESENCHYMAL TRANSITION; ENDOTHELIUM CELL; EPITHELIAL MESENCHYMAL TRANSITION; EYE DEVELOPMENT; EYEBALL; HOMEOSTASIS; MESENCHYME CELL; MOUSE; MYOFIBROBLAST; NONHUMAN; POSTNATAL DEVELOPMENT; PRENATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; STRESS FIBER; TRANSGENIC MOUSE; WOUND HEALING;

ACTINS; ANIMALS; ANIMALS, NEWBORN; CADHERINS; CELL DIFFERENTIATION; CORNEAL STROMA; FIBROBLASTS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MICE; MICE, TRANSGENIC; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1;

EID: 73149100784     PISSN: 03619230     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainresbull.2009.10.019     Document Type: Article

References (77)

1. Akhurst R.J. TGF beta signaling in health and disease. Nat. Genet. 36 (2004) 790-792
2. Akhurst R.J., and Derynck R. TGF-beta signaling in cancer-a double-edged sword. Trends Cell Biol. 11 (2001) S44-S51
3. Carrington L.M., Albon J., Anderson I., Kamma C., and Boulton M. Differential regulation of key stages in early corneal wound healing by TGF-beta isoforms and their inhibitors. Invest. Ophthalmol. Vis. Sci. 47 (2006) 1886-1894
4. Chen C., Michelini-Norris B., Stevens S., Rowsey J., Ren X., Goldstein M., and Schultz G. Measurement of mRNAs for TGFss and extracellular matrix proteins in corneas of rats after PRK. Invest. Ophthalmol. Vis. Sci. 41 (2000) 4108-4116
5. Cutroneo K.R. TGF-beta-induced fibrosis and SMAD signaling: oligo decoys as natural therapeutics for inhibition of tissue fibrosis and scarring. Wound Repair Regen. 15 Suppl. 1 (2007) S54-S60
6. Czaja M.J., Weiner F.R., Flanders K.C., Giambrone M.A., Wind R., Biempica L., and Zern M.A. In vitro and in vivo association of transforming growth factor-beta 1 with hepatic fibrosis. J. Cell Biol. 108 (1989) 2477-2482
7. de Iongh R.U., Gordon-Thomson C., Chamberlain C.G., Hales A.M., and McAvoy J.W. Tgfbeta receptor expression in lens: implications for differentiation and cataractogenesis. Exp. Eye Res. 72 (2001) 649-659
8. de Iongh R.U., Wederell E., Lovicu F.J., and McAvoy J.W. Transforming growth factor-beta-induced epithelial-mesenchymal transition in the lens: a model for cataract formation. Cells Tissues Organs 179 (2005) 43-55 (179(1-2) 43-55)
9. Derynck R., and Zhang Y.E. Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature 425 (2003) 577-584
10. Dunker N., and Krieglstein K. Reduced programmed cell death in the retina and defects in lens and cornea of Tgfbeta2(-/-) Tgfbeta3(-/-) double-deficient mice. Cell Tissue Res. 313 (2003) 1-10
11. Esquenazi S., He J., Bazan N.G., and Bazan H.E. Comparison of corneal wound-healing response in photorefractive keratectomy and laser-assisted subepithelial keratectomy. J. Cataract Refract. Surg. 31 (2005) 1632-1639
12. Flugel-Koch C., Ohlmann A., Piatigorsky J., and Tamm E.R. Disruption of anterior segment development by TGF-beta1 overexpression in the eyes of transgenic mice. Dev. Dyn. 225 (2002) 111-125
13. Fromm L., Shawlot W., Gunning K., Butel J.S., and Overbeek P.A. The retinoblastoma protein-binding region of simian virus 40 large T antigen alters cell cycle regulation in lenses of transgenic mice. Mol. Cell. Biol. 14 (1994) 6743-6754
14. Garana R.M., Petroll W.M., Chen W.T., Herman I.M., Barry P., Andrews P., Cavanagh H.D., and Jester J.V. Radial keratotomy. II. Role of the myofibroblast in corneal wound contraction. Invest. Ophthalmol. Vis. Sci. 33 (1992) 3271-3282
15. Gordon-Thomson C., de Iongh R.U., Hales A.M., Chamberlain C.G., and McAvoy J.W. Differential cataractogenic potency of TGF-beta1, -beta2, and -beta3 and their expression in the postnatal rat eye. Invest. Ophthalmol. Vis. Sci. 39 (1998) 1399-1409
16. Gumbiner B.M. Regulation of cadherin-mediated adhesion in morphogenesis. Nat. Rev. Mol. Cell Biol. 6 (2005) 622-634
17. Gupta A., Monroy D., Ji Z., Yoshino K., Huang A., and Pflugfelder S.C. Transforming growth factor beta-1 and beta-2 in human tear fluid. Curr. Eye Res. 15 (1996) 605-614
18. Hales A.M., Chamberlain C.G., and McAvoy J.W. Cataract induction in lenses cultured with transforming growth factor-beta. Invest. Ophthalmol. Vis. Sci. 36 (1995) 1709-1713
19. He J., and Bazan H.E. Epidermal growth factor synergism with TGF-beta1 via PI-3 kinase activity in corneal keratocyte differentiation. Invest. Ophthalmol. Vis. Sci. 49 (2008) 2936-2945
20. Helbig H., Kittredge K.L., Coca-Prados M., Davis J., Palestine A.G., and Nussenblatt R.B. Mammalian ciliary-body epithelial cells in culture produce transforming growth factor-beta. Graefes. Arch. Clin. Exp. Ophthalmol. 229 (1991) 84-87
21. Heldin C.H., Landstrom M., and Moustakas A. Mechanism of TGF-beta signaling to growth arrest, apoptosis, and epithelial-mesenchymal transition. Curr. Opin. Cell Biol. 21 (2009) 166-176
22. Imanishi J., Kamiyama K., Iguchi I., Kita M., Sotozono C., and Kinoshita S. Growth factors: importance in wound healing and maintenance of transparency of the cornea. Prog. Retin. Eye Res. 19 (2000) 113-129
23. Ittner L.M., Wurdak H., Schwerdtfeger K., Kunz T., Ille F., Leveen P., Hjalt T.A., Suter U., Karlsson S., Hafezi F., Born W., and Sommer L. Compound developmental eye disorders following inactivation of TGFbeta signaling in neural-crest stem cells. J. Biol. 4 (2005) 11
24. Jampel H.D., Roche N., Stark W.J., and Roberts A.B. Transforming growth factor-beta in human aqueous humor. Curr. Eye Res. 9 (1990) 963-969
25. Jester J.V., Barry-Lane P.A., Petroll W.M., Olsen D.R., and Cavanagh H.D. Inhibition of corneal fibrosis by topical application of blocking antibodies to TGF beta in the rabbit. Cornea 16 (1997) 177-187
26. Jester J.V., Huang J., Petroll W.M., and Cavanagh H.D. TGFbeta induced myofibroblast differentiation of rabbit keratocytes requires synergistic TGFbeta, PDGF and integrin signaling. Exp. Eye Res. 75 (2002) 645-657
27. Jester J.V., Petroll W.M., Barry P.A., and Cavanagh H.D. Expression of alpha-smooth muscle (alpha-SM) actin during corneal stromal wound healing. Invest. Ophthalmol. Vis. Sci. 36 (1995) 809-819
28. Jester J.V., Petroll W.M., Barry P.A., and Cavanagh H.D. Temporal, 3-dimensional, cellular anatomy of corneal wound tissue. J. Anat. 186 Pt 2 (1995) 301-311
29. Joyce N.C., Harris D.L., and Mello D.M. Mechanisms of mitotic inhibition in corneal endothelium: contact inhibition and TGF-beta2. Invest. Ophthalmol. Vis. Sci. 43 (2002) 2152-2159
30. Joyce N.C., and Zieske J.D. Transforming growth factor-beta receptor expression in human cornea. Invest. Ophthalmol. Vis. Sci. 38 (1997) 1922-1928
31. Kaartinen V., Voncken J.W., Shuler C., Warburton D., Bu D., Heisterkamp N., and Groffen J. Abnormal lung development and cleft palate in mice lacking TGF-beta 3 indicates defects of epithelial-mesenchymal interaction. Nat. Genet. 11 (1995) 415-421
32. Kaji Y., Mita T., Obata H., Tsuru T., Soya K., Shirasawa E., Sakai H., Hanyu A., Kato M., and Yamashita H. Expression of transforming growth factor beta superfamily and their receptors in the corneal stromal wound healing process after excimer laser keratectomy. Br. J. Ophthalmol. 82 (1998) 462-463
33. Kaji Y., Soya K., Amano S., Oshika T., and Yamashita H. Relation between corneal haze and transforming growth factor-beta1 after photorefractive keratectomy and laser in situ keratomileusis. J. Cataract Refract. Surg. 27 (2001) 1840-1846
34. Kao W.W., Xia Y., Liu C.Y., and Saika S. Signaling pathways in morphogenesis of cornea and eyelid. Ocul. Surf. 6 (2008) 9-23
35. Kaur H., Chaurasia S.S., Agrawal V., and Wilson S.E. Expression of PDGF receptor alpha in corneal myofibroblasts in situ. Exp. Eye Res. 89 (2009) 432-434
36. Kulkarni A.B., Huh C.G., Becker D., Geiser A., Lyght M., Flanders K.C., Roberts A.B., Sporn M.B., Ward J.M., and Karlsson S. Transforming growth factor beta 1 null mutation in mice causes excessive inflammatory response and early death. Proc. Natl. Acad. Sci. U.S.A. 90 (1993) 770-774
37. Kurosaka D., and Nagamoto T. Inhibitory effect of TGF-beta 2 in human aqueous humor on bovine lens epithelial cell proliferation. Invest. Ophthalmol. Vis. Sci. 35 (1994) 3408-3412
38. Lee J.G., and Kay E.P. FGF-2-induced wound healing in corneal endothelial cells requires Cdc42 activation and Rho inactivation through the phosphatidylinositol 3-kinase pathway. Invest. Ophthalmol. Vis. Sci. 47 (2006) 1376-1386
39. Lovicu F.J., Schulz M.W., Hales A.M., Vincent L.N., Overbeek P.A., Chamberlain C.G., and McAvoy J.W. TGFbeta induces morphological and molecular changes similar to human anterior subcapsular cataract. Br. J. Ophthalmol. 86 (2002) 220-226
40. Lutty G.A., Merges C., Threlkeld A.B., Crone S., and McLeod D.S. Heterogeneity in localization of isoforms of TGF-beta in human retina, vitreous, and choroid. Invest. Ophthalmol. Vis. Sci. 34 (1993) 477-487
41. Massague J. TGF-beta signal transduction. Ann. Rev. Biochem. 67 (1998) 753-791
42. Massague J. TGFbeta in Cancer. Cell 134 (2008) 215-230
43. Massague J., and Chen Y.G. Controlling TGF-beta signaling. Genes Dev. 14 (2000) 627-644
44. Massague J., and Gomis R.R. The logic of TGFbeta signaling. FEBS Lett. 580 (2006) 2811-2820
45. Masur S.K., Conors Jr. R.J., Cheung J.K., and Antohi S. Matrix adhesion characteristics of corneal myofibroblasts. Invest. Ophthalmol. Vis. Sci. 40 (1999) 904-910
46. Masur S.K., Dewal H.S., Dinh T.T., Erenburg I., and Petridou S. Myofibroblasts differentiate from fibroblasts when plated at low density. Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 4219-4223
47. Millan F.A., Denhez F., Kondaiah P., and Akhurst R.J. Embryonic gene expression patterns of TGF beta 1, beta 2 and beta 3 suggest different developmental functions in vivo. Development 111 (1991) 131-143
48. Mita T., Yamashita H., Kaji Y., Obata H., Hanyu A., Suzuki M., and Tobari I. Functional difference of TGF-beta isoforms regulating corneal wound healing after excimer laser keratectomy. Exp. Eye Res. 68 (1999) 513-519
49. Nishida K., Kinoshita S., Yokoi N., Kaneda M., Hashimoto K., and Yamamoto S. Immunohistochemical localization of transforming growth factor-beta 1, -beta 2, and -beta 3 latency-associated peptide in human cornea. Invest. Ophthalmol. Vis. Sci. 35 (1994) 3289-3294
50. Obata H., Kaji Y., Yamada H., Kato M., Tsuru T., and Yamashita H. Expression of transforming growth factor-beta superfamily receptors in rat eyes. Acta Ophthalmol. Scand. 77 (1999) 151-156
51. Okazaki M., Takeshita S., Kawai S., Kikuno R., Tsujimura A., Kudo A., and Amann E. Molecular cloning and characterization of OB-cadherin, a new member of cadherin family expressed in osteoblasts. J. Biol. Chem. 269 (1994) 12092-12098
52. Padua D., and Massague J. Roles of TGFbeta in metastasis. Cell Res. 19 (2009) 89-102
53. Pasquale L.R., Dorman-Pease M.E., Lutty G.A., Quigley H.A., and Jampel H.D. Immunolocalization of TGF-beta 1, TGF-beta 2, and TGF-beta 3 in the anterior segment of the human eye. Invest. Ophthalmol. Vis. Sci. 34 (1993) 23-30
54. Pelton R.W., Saxena B., Jones M., Moses H.L., and Gold L.I. Immunohistochemical localization of TGF beta 1, TGF beta 2, and TGF beta 3 in the mouse embryo: expression patterns suggest multiple roles during embryonic development. J. Cell Biol. 115 (1991) 1091-1105
55. Piek E., Heldin C.H., and Ten Dijke P. Specificity, diversity, and regulation in TGF-beta superfamily signaling. FASEB J. 13 (1999) 2105-2124
56. Pishvaian M.J., Feltes C.M., Thompson P., Bussemakers M.J., Schalken J.A., and Byers S.W. Cadherin-11 is expressed in invasive breast cancer cell lines. Cancer Res. 59 (1999) 947-952
57. Proetzel G., Pawlowski S.A., Wiles M.V., Yin M., Boivin G.P., Howles P.N., Ding J., Ferguson M.W., and Doetschman T. Transforming growth factor-beta 3 is required for secondary palate fusion. Nat. Genet. 11 (1995) 409-414
58. Roberts A.B., and Wakefield L.M. The two faces of transforming growth factor beta in carcinogenesis. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 8621-8623
59. Robertson J.V., Nathu Z., Najjar A., Dwivedi D., Gauldie J., and West-Mays J.A. Adenoviral gene transfer of bioactive TGFbeta1 to the rodent eye as a novel model for anterior subcapsular cataract. Mol. Vis. 13 (2007) 457-469
60. Saika S. TGFbeta pathobiology in the eye. Lab. Invest. 86 (2006) 106-115
61. Saika S., Liu C.Y., Azhar M., Sanford L.P., Doetschman T., Gendron R.L., Kao C.W., and Kao W.W. TGFbeta2 in corneal morphogenesis during mouse embryonic development. Dev. Biol. 240 (2001) 419-432
62. Saika S., Yamanaka O., Sumioka T., Miyamoto T., Miyazaki K., Okada Y., Kitano A., Shirai K., Tanaka S., and Ikeda K. Fibrotic disorders in the eye: targets of gene therapy. Prog. Retin. Eye Res. 27 (2008) 177-196
63. Sanford L.P., Ormsby I., Gittenberger-de Groot A.C., Sariola H., Friedman R., Boivin G.P., Cardell E.L., and Doetschman T. TGFbeta2 knockout mice have multiple developmental defects that are non-overlapping with other TGFbeta knockout phenotypes. Development 124 (1997) 2659-2670
64. Savagner P. Leaving the neighborhood: molecular mechanisms involved during epithelial-mesenchymal transition. Bioessays 23 (2001) 912-923
65. Schmierer B., and Hill C.S. TGFbeta-SMAD signal transduction: molecular specificity and functional flexibility. Nat. Rev. Mol. Cell Biol. 8 (2007) 970-982
66. Schulz M.W., Chamberlain C.G., and McAvoy J.W. Inhibition of transforming growth factor-beta-induced cataractous changes in lens explants by ocular media and alpha 2-macroglobulin. Invest. Ophthalmol. Vis. Sci. 37 (1996) 1509-1519
67. Shull M.M., Ormsby I., Kier A.B., Pawlowski S., Diebold R.J., Yin M., Allen R., Sidman C., Proetzel G., Calvin D., et al. Targeted disruption of the mouse transforming growth factor-beta 1 gene results in multifocal inflammatory disease. Nature 359 (1992) 693-699
68. Srinivasan Y., Lovicu F.J., and Overbeek P.A. Lens-specific expression of transforming growth factor beta1 in transgenic mice causes anterior subcapsular cataracts. J. Clin. Invest. 101 (1998) 625-634
69. Tomita K., van Bokhoven A., van Leenders G.J., Ruijter E.T., Jansen C.F., Bussemakers M.J., and Schalken J.A. Cadherin switching in human prostate cancer progression. Cancer Res. 60 (2000) 3650-3654
70. Vesaluoma M., Teppo A.M., Gronhagen-Riska C., and Tervo T. Release of TGF-beta 1 and VEGF in tears following photorefractive keratectomy. Curr. Eye Res. 16 (1997) 19-25
71. Wheelock M.J., Shintani Y., Maeda M., Fukumoto Y., and Johnson K.R. Cadherin switching. J. Cell Sci. 121 (2008) 727-735
72. Wilson S.E., Chen L., Mohan R.R., Liang Q., and Liu J. Expression of HGF, KGF, EGF and receptor messenger RNAs following corneal epithelial wounding. Exp. Eye Res. 68 (1999) 377-397
73. Xu L., Overbeek P.A., and Reneker L.W. Systematic analysis of E-, N- and P-cadherin expression in mouse eye development. Exp. Eye Res. 74 (2002) 753-760
74. Yagi T., and Takeichi M. Cadherin superfamily genes: functions, genomic organization, and neurologic diversity. Genes Dev. 14 (2000) 1169-1180
75. Yamamoto T., Noble N.A., Miller D.E., and Border W.A. Sustained expression of TGF-beta 1 underlies development of progressive kidney fibrosis. Kidney Int. 45 (1994) 916-927
76. Zhao S., and Overbeek P.A. Elevated TGFbeta signaling inhibits ocular vascular development. Dev. Biol. 237 (2001) 45-53
77. Zieske J.D., Hutcheon A.E., Guo X., Chung E.H., and Joyce N.C. TGF-beta receptor types I and II are differentially expressed during corneal epithelial wound repair. Invest. Ophthalmol. Vis. Sci. 42 (2001) 1465-1471