Smad3 is required for dedifferentiation of retinal pigment epithelium following retinal detachment in mice

Laboratory Investigation

Volumn 84, Issue 10, 2004, Pages 1245-1258

  Saika, Shizuya ^a   Kono Saika, Satoko ^a   Tanaka, Takeshi ^a   Yamanaka, Osamu ^a   Ohnishi, Yoshitaka ^a   Sato, Misako ^a   Muragaki, Yasuteru ^a   Ooshima, Akira ^a   Yoo, Jiyun ^b   Flanders, Kathleen C ^b,c   Roberts, Anita B ^b  

^a WAKAYAMA MEDICAL UNIVERSITY   (Japan)

^b NATIONAL CANCER INSTITUTE   (United States)

^c Gyeongsang National University   (South Korea)

Author keywords

Epithelial mesenchymal transition; Mouse; Proliferative vitreoretinopathy; Retinal pigment epithelial cell; Smad; Transforming growth factor

Indexed keywords

ACTIVIN RECEPTOR; ALPHA ACTIN; COLLAGEN TYPE 6; LUMICAN; PLATELET DERIVED GROWTH FACTOR BB; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; ACTIN; BIOLOGICAL MARKER; DNA BINDING PROTEIN; KERATAN SULFATE; PLATELET DERIVED GROWTH FACTOR; PLATELET-DERIVED GROWTH FACTOR BB; PROTEOCHONDROITIN SULFATE; SMAD3 PROTEIN, HUMAN; SMAD3 PROTEIN, MOUSE; TGFB2 PROTEIN, HUMAN; TRANSACTIVATOR PROTEIN; TRANSFORMING GROWTH FACTOR BETA2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DOWNSTREAM PROCESSING; EPITHELIUM CELL; FIBROSIS; MESENCHYME CELL; MOUSE; NONHUMAN; NULL ALLELE; PRIORITY JOURNAL; PROLIFERATIVE RETINOPATHY; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RETINA DETACHMENT; SIGNAL TRANSDUCTION; VITRECTOMY; ANIMAL; BIOSYNTHESIS; CELL LINE; CELL MOTION; DISEASE MODEL; DRUG EFFECT; FLUORESCENT ANTIBODY TECHNIQUE; HUMAN; METABOLISM; MOUSE MUTANT; MOUSE STRAIN; PATHOLOGY; PHYSIOLOGY; PIGMENT EPITHELIUM; SWINE; VITREORETINOPATHY;

ACTINS; ANIMALS; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL LINE; CELL MOVEMENT; COLLAGEN TYPE VI; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; HUMANS; KERATAN SULFATE; MICE; MICE, INBRED STRAINS; MICE, KNOCKOUT; PIGMENT EPITHELIUM OF EYE; PLATELET-DERIVED GROWTH FACTOR; PROTEOCHONDROITIN SULFATES; RETINAL DETACHMENT; SIGNAL TRANSDUCTION; SMAD3 PROTEIN; SWINE; TRANS-ACTIVATORS; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA2; VITREORETINOPATHY, PROLIFERATIVE;

EID: 4944259825     PISSN: 00236837     EISSN: None     Source Type: Journal    
DOI: 10.1038/labinvest.3700156     Document Type: Article

References (56)

1. Pastor JC, de la Rua ER, Martin F. Proliferative vitreoretinopathy: risk factors and pathobiology. Prog Retin Eye Res 2002;21:127-144.
2. Casaroli-Marano RP, Pagan R, Vilaro S. Epithelial-mesenchymal transition in proliferative vitreoretinopathy: intermediate filament protein expression in retinal pigment epithelial cells. Invest Ophthalmol Vis Sci 1999;40:2062-2072.
3. Sheridan CM, Occleston NL, Hiscott P, et al. Matrix metalloproteinases: a role in the contraction of vitreoretinal scar tissue. Am J Pathol 2001;159:1555-1566.
4. Grisanti S, Guidry C. Transdifferentiation of retinal pigment epithelial cells from epithelial to mesenchymal phenotype. Invest Ophthalmol Vis Sci 1995;36: 391-405.
5. Lee SC, Kwon OW, Seong GJ, et al. Epitheliomesenchymal transdifferentiation of cultured RPE cells. Ophthalmic Res 2001;33:80-86.
6. Cassidy L, Barry P, Shaw C, et al. Platelet derived growth factor and fibroblast growth factor basic levels in the vitreous of patients with vitreoretinal disorders. Br J Ophthalmol 1998;82:181-185.
7. Hinton DR, He S, Jin ML, et al. Novel growth factors involved in the pathogenesis of proliferative vitreoretinopathy. Eye 2002;16:422-428.
8. Kon CH, Occleston NL, Aylward GW, et al. Expression of vitreous cytokines in proliferative vitreoretinopathy: a prospective study. Invest Ophthalmol Vis Sci 1999;40:705-712.
9. Liang X, Li C, Li Y, et al. Platelet-derived growth factor and basic fibroblast growth factor immunolocalized in proliferative retinal diseases. Chin Med J 2000;113: 144-147.
10. Yamamoto T, Takeuchi S, Suzuki K, et al. Expression and possible roles of activin A in proliferative vitreoretinal diseases. Jpn J Ophthalmol 2000;44: 221-226.
11. Bochaton-Piallat ML, Kapetanios AD, Donati G, et al. TGF-β1, TGF-β receptor II and ED-A fibronectin expression in myofibroblast of vitreoretinopathy. Invest Ophthalmol Vis Sci 2000;41:2336-2342.
12. Connor Jr TB, Roberts AB, Sporn MB, et al. Correlation of fibrosis and transforming growth factor-beta type 2 levels in the eye. J Clin Invest 1989;83:1661-1666.
13. Bhowmick NA, Ghiassi M, Bakin A, et al. Transforming growth factor-b1 mediates epithelial to mesenchymal transdifferentiation through a RhoA-dependent mechanism. Mol Biol Cell 2001;12:27-36.
14. Nicolas FJ, Lehmann K, Warne PH, et al. Epithelial to mesenchymal transition in Madin-Darby canine kidney cells is accompanied by down-regulation of Smad3 expression, leading to resistance to transforming growth factor-beta-induced growth arrest. J Biol Chem 2003;278:3251-3256.
15. Janda E, Lehmann K, Killisch I, et al. Ras and TGF-β cooperatively regulate epithelial cell plasticity and metastasis: dissection of Ras signaling pathways. J Cell Biol 2002;156:299-314.
16. Oft M, Akhurst RJ, Balmain A. Metastasis is driven by sequential elevation of H-ras and Smad2 levels. Nat Cell Biol 2002;4:487-494.
17. Pfeffer BA, Flanders KC, Guerin CJ, et al. Transforming growth factor β2 is the predominant isoform in the neural retina, retinal pigment epithelium-choroid and vitreous of the monkey eye. Exp Eye Res 1994;59:323-333.
18. Kurosaka D, Muraki Y, Inoue M, et al. TGF-β2 increases alpha-smooth muscle actin expression in bovine retinal pigment epithelial cells. Curr Eye Res 1996;15:1144-1147.
19. Stocks SZ, Taylor SM, Shiels IA. Transforming growth factor-β1 induces a-smooth muscle actin expression and fibronectin synthesis in cultured human retinal pigment epithelial cells. Clin Experiment Ophthalmol 2001;29:33-37.
20. Battegay EJ, Raines EW, Seifert RA, et al. TGF-β induces bimodal proliferation of connective tissue cells via complex control of an autocrine PDGF loop. Cell 1990;63:515-524.
21. Bronzert DA, Bates SE, Sheridan JP, et al. Transforming growth factor-β induces platelet-derived growth factor (PDGF) messenger RNA and PDGF secretion while inhibiting growth in normal human mammary epithelial cells. Mol Endocrinol 1990;4:981-989.
22. Choudhury P, Chen W, Hunt RC. Production of platelet-derived growth factor by interleukin-1β and transforming growth factor-β-stimulated retinal pigment epithelial cells leads to contraction of collagen gels. Invest Ophthalmol Vis Sci 1997;38:824-833.
23. Leask A, Holmes A, Black CM, et al. CTGF gene regulation: requirements for its induction by TGFβ2 in fibroblasts. J Biol Chem 2003;278:13008- 13015.
24. Piek E, Roberts AB. Suppressor and oncogenic roles of transforming growth factor-beta and its signaling pathways in tumorigenesis. Adv Cancer Res 2001;83: 1-54.
25. Shi Y, Massague J. Mechanisms of TGF-β signaling from cell membrane to the nucleus. Cell 2003;113:685-700.
26. ten Dijke P, Goumans MJ, Itoh F, et al. Regulation of cell proliferation by Smad proteins. J Cell Physiol 2002;191:1-16.
27. Bakin AV, Tomlinson AK, Bhowmick NA, et al. Phosphatidylinositol 3-kinase function is required for transforming growth factor β-mediated epithelial to mesenchymal transition and cell migration. J Biol Chem 2000;275:36803-36810.
28. Oft M, Peli J, Rudaz C, et al. TGF-β1 and Ha-Ras collaborate in modulating the phenotypic plasticity and invasiveness of epithelial tumor cells. Genes Dev 1996;10:2462-2477.
29. Itoh S, Thorikay M, Kowanetz M, et al. Elucidation of Smad requirement in transforming growth factor-β type I receptor-induced responses. J Biol Chem 2003;278:3751-3761.
30. Yu L, Hebert MC, Zhang YE. TGF-β receptor-activated p38 MAP kinase mediates Smad-independent TGF-beta responses. EMBO J 2002;21:3749-3759.
31. Yang X, Letterio JJ, Lechleider RJ, et al. Targeted disruption of SMAD3 results in impaired mucosal immunity and diminished T cell responsiveness to TGF-β. EMBO J 1999;18:1280-1291.
32. Saika S, Kono-Saika S, Tanaka S, et al. Smad3 signaling is required for epithelial-mesenchymal transition of lens epithelium after injury. Am J Pathol 2003;164:651-663.
33. Sato M, Muragaki Y, Saika S, et al. Targeted disruption of TGF-β/Smad3 signaling protects against renal tubulointerstitial fibrosis induced by unilateral ureteral obstruction. J Clin Invest 2003;112:1486-1494.
34. Dunn KC, Aotaki-Keen AE, Putkey FR, et al. ARPE-19, a human retinal pigment epithelial cell line with differentiated properties. Exp Eye Res 1996;62: 155-169.
35. Martini B, Pandey R, Ogden TE. Cultures of human retinal pigment epithelium. Modulation of extracellular matrix. Invest Ophthalmol Vis Sci 1992;33: 516-521.
36. Saika S, Shiraishi A, Liu CY, et al. Role of lumican in the corneal epithelium during wound healing. J Biol Chem 2000;275:2607-2612.
37. Saika S, Saika S, Liu CY, et al. TGFβ2 in corneal morphogenesis during mouse embryonic development. Dev Biol 2001;240:419-432.
38. Saika S, Ooshima A, Hashizume N, et al. Effect of lysyl hydroxylase inhibitor, minoxidil, on ultrastructure and behavior of cultured rabbit subconjunctival fibroblasts. Graefes Arch Clin Exp Ophthalmol 1995;233:347-353.
39. Ohno-Matsui K, Hirose A, Yamamoto S, et al. Inducible expression of vascular endothelial growth factor in adult mice causes severe proliferative retinopathy and retinal detachment. Am J Pathol 2002;160:711-719.
40. Seo MS, Okamoto N, Vinores MA, et al. Photoreceptor-specific expression of platelet-derived growth factor-B results in traction retinal detachment. Am J Pathol 2000;157:995-1005.
41. Yeo JH, Sadeghi J, Campochiaro PA, et al. Intravitreous fibronectin and platelet-derived growth factor. New model for traction retinal detachment. Arch Ophthalmol 1986;104:417-421.
42. Hisatomi T, Sakamoto T, Murata T, et al. Relocalization of apoptosis-inducing factor in photoreceptor apoptosis induced by retinal detachment in vivo. Am J Pathol 2001;158:1271-1278.
43. Oshima Y, Sakamoto T, Hisatomi T, et al. Gene transfer of soluble TGF-β type II receptor inhibits experimental proliferative vitreoretinopathy. Gene Therapy 2002;9: 1214-1220.
44. Ikuno Y, Kazlauskas A. An in vivo gene therapy approach for experimental proliferative vitreoretinopathy using the truncated platelet-derived growth factor alpha receptor. Invest Ophthalmol Vis Sci 2002;43:2406-2411.
45. Valeria Canto SM, Gallo JE, Dodds RA, et al. A mouse model of proliferative vitreoretinopathy induced by dispase. Exp Eye Res 2002;75:491-504.
46. Anderson DH, Guerin CJ, Erickson PA, et al. Morphological recovery in the reattached retina. Invest Ophthalmol Vis Sci 1986;27:168-183.
47. Ando A, Ueda M, Uyama M, et al. Enhancement of dedifferentiation and myoid differentiation of retinal pigment epithelial cells by platelet derived growth factor. Br J Ophthalmol 2000;84:1306-1311.
48. Saika S, Miyamoto T, Tanaka S, et al. Response of lens epithelial cells to injury: role of lumican in epithelial-mesenchymal transition. Invest Ophthalmol Vis Sci 2003;44:2094-2102.
49. Knupp C, Amin SZ, Munro PM, et al. Collagen VI assemblies in age-related macular degeneration. J Struct Biol 2002;139:181-189.
50. Saika S, Miyamoto T, Ishida I, et al. TGFβ-Smad signalling in postoperative human lens epithelial cells. Br J Ophthalmol 2002;86:1428-1433.
51. Somasundaram R, Schuppan D. Type I, II, III, IV, V, and VI collagens serve as extracellular ligands for the isoforms of platelet-derived growth factor (AA, BB, and AB). J Biol Chem 1996;271:26884-26891.
52. Jaffe GJ, Harrison CE, Lui GM, et al. Activin expression by cultured human retinal pigment epithelial cells. Invest Ophthalmol Vis Sci 1994;35:2924-2931.
53. Roberts AB, Sporn MB. The transforming growth factors-β. In: Sporn MB, Roberts AB (eds). Handbook of Experimental Pharmacology. Peptide Growth Factors and Their Receptors. Springer-Verlag: New York, 1990, pp 419-472.
54. Carrington L, McLeod D, Boulton M. IL-10 and antibodies to TGF-β2 and PDGF inhibit RPE-mediated retinal contraction. Invest Ophthalmol Vis Sci 2000; 41:1210-1216.
55. Sintich SM, Lamm ML, Sensibar JA, et al. Transforming growth factor-b1-induced proliferation of the prostate cancer cell line, TSU-Pr1: the role of platelet-derived growth factor. Endocrinology 1999;140: 3411-3415.
56. Taylor LM, Khachigian LM. Induction of platelet-derived growth factor B-chain expression by transforming growth factor-β involves transactivation by Smads. J Biol Chem 2000;275:16709-16716.