Activation of Smad-mediated TGF-β signaling triggers epithelial-mesenchymal transitions in murine cloned corneal progenitor cells

Journal of Cellular Physiology

Volumn 228, Issue 1, 2013, Pages 225-234

  Kawakita, Tetsuya ^a,b,c   Espana, Edgar M ^a   Higa, Kazunari ^b,c   Kato, Naoko ^c   Li, Wei ^a   Tseng, Scheffer C G ^a  

^a OCULAR SURFACE CENTER   (United States)

^b TOKYO DENTAL COLLEGE   (Japan)

^c KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; BETA CATENIN; CALVASCULIN; CYCLINE; CYTOKERATIN 14; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 1ALPHA; LYMPHOID ENHANCER FACTOR 1; NEUTRALIZING ANTIBODY; PROTEIN P63; SMAD PROTEIN; SMAD4 PROTEIN; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAIL; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1; UVOMORULIN; WNT PROTEIN;

ANIMAL CELL; ARTICLE; CELL CLONE; CELL DENSITY; CELL DIFFERENTIATION; CELL JUNCTION; CELL NUCLEUS; COLONY FORMATION; CONTROLLED STUDY; CORNEA LIMBUS; CORNEAL PROGENITOR CELL; CYTOPLASM; EMBRYO DEVELOPMENT; EPITHELIAL MESENCHYMAL TRANSITION; EXPLANT; MOUSE; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STEM CELL;

ACTINS; ANIMALS; ANTIBODIES, NEUTRALIZING; BETA CATENIN; CELL DIFFERENTIATION; CELLS, CULTURED; CORNEA; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; INTERLEUKIN-1ALPHA; MESENCHYMAL STROMAL CELLS; MICE; SMAD PROTEINS; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA2; WNT PROTEINS;

MURINAE;

EID: 84867186245     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.24126     Document Type: Article

References (59)

1. Barnard JA, Bascom CC, Lyon RM, Sipes NJ, Moses HL. 1988. Transforming growth factor-β in the control of epidermal proliferation. Am J Med Sci 31: 159-163.
2. Caldelari R, Suter MM, Baumann D, De Bruin A, Muller E. 2000. Long-term culture of murine epidermal keratinocytes. J Invest Dermatol 114: 1064-1065.
3. Chagraoui J, Lepage-Noll A, Anjo A, Uzan G, Charbord P. 2003. Fetal liver stroma consists of cells in epithelial-to-mesenchymal transition. Blood 101: 2973-2982.
4. Chilosi M, Poletti V, Zamo A, Lestani M, Montagna L, Piccoli P, Pedron S, Bertaso M, Scarpa A, Murer B, Cancellieri A, Maestro R, Semenzato G, Doglioni C. 2003. Aberrant Wnt/beta-catenin pathway activation in idiopathic pulmonary fibrosis. Am J Pathol 162: 1495-1502.
5. Dietrich C, Scherwat J, Faust D, Oesch F. 2002. Subcellular localization of beta-catenin is regulated by cell density. Biochem Biophys Res Commun 292: 195-199.
6. Fan JM, Ng YY, Hill PA, Nikolic-Paterson DJ, Mu W, Atkins RC, Lan HY. 1999. Transforming growth factor-beta regulates tubular epithelial-myofibroblast transdifferentiation in vitro. Kidney Int 56: 1455-1467.
7. Forino M, Torregrossa R, Ceol M, Murer L, Vella MD, Prete DD, D'Angelo A, Anglani F. 2006. TGFbeta1 induces epithelial-mesenchymal transition, but not myofibroblast transdifferentiation of human kidney tubular epithelial cells in primary culture. Int J Exp Pathol 87: 197-208.
8. Grigorian M, Andresen S, Tulchinsky E, Kriajevska M, Carlberg C, Kruse C, Cohn M, Ambartsumian N, Christensen A, Selivanova G, Lukanidin E. 2001. Tumor suppressor p53 protein is a new target for the metastasis-associated Mts1/S100A4 protein: Functional consequences of their interaction. J Biol Chem 276: 22699-22708.
9. Hager B, Bickenbach JR, Fleckman P. 1999. Long-term culture of murine epidermal keratinocytes 112: 971-976.
10. He XC, Zhang J, Tong WG, Tawfik O, Ross J, Scoville DH, Tian Q, Zeng X, He X, Wiedemann LM, Mishina Y, Li L. 2004. BMP signaling inhibits intestinal stem cell self-renewal through suppression of Wnt-beta-catenin signaling. Nat Genet 36: 1117-1121.
11. Heng BC, Cao T, Liu H, Phan TT. 2005. Directing stem cells into the keratinocyte lineage in vitro. Exp Dermatol 14: 1-16.
12. Iwano M, Plieth D, Danoff TM, Xue C, Okada H, Neilson EG. 2002. Evidence that fibroblasts derive from epithelium during tissue fibrosis. J Clin Invest 110: 341-350.
13. Jamora C, DasGupta R, Kocieniewski P, Fuchs E. 2003. Links between signal transduction, transcription and adhesion in epithelial bud development. Nature 422: 317-322.
14. Kalluri R, Neilson EG. 2003. Epithelial-mesenchymal transition and its implications for fibrosis. J Clin Invest 112: 1776-1784.
15. Kawakita T, Espana EM, He H, Yeh LK, Liu CY, Tseng SC. 2004. Calcium-induced abnormal epidermal-like differentiation in cultures of mouse corneal-limbal epithelial cells. Invest Ophthalmol Vis Sci 45: 3507-3512.
16. Kawakita T, Espana EM, He H, Li W, Liu CY, Tseng SC. 2005. Intrastromal invasion by limbal epithelial cells is mediated by epithelial-mesenchymal transition activated by air exposure. Am J Pathol 167: 381-393.
17. Kim K, Lu Z, Hay ED. 2002. Direct evidence for a role of beta-catenin/LEF-1 signaling pathway in induction of EMT. Cell Biol Int 26: 463-476.
18. Kim KK, Kugler MC, Wolters PJ, Robillard L, Galvez MG, Brumwell AN, Sheppard D, Chapman HA. 2006. Alveolar epithelial cell mesenchymal transition develops in vivo during pulmonary fibrosis and is regulated by the extracellular matrix. Proc Natl Acad Sci USA 103: 13180-13185.
19. Kruse FE, Tseng SCG. 1992. Proliferative and differentiative response of corneal and limbal epithelium to extracellular calcium in serum-free cultures. J Cell Physiol 151: 347-360.
20. Kuhnert F, Davis CR, Wang HT, Chu P, Lee M, Yuan J, Nusse R, Kuo CJ. 2004. Essential requirement for Wnt signaling in proliferation of adult small intestine and colon revealed by adenoviral expression of Dickkopf-1. Proc Natl Acad Sci USA 101: 266-271.
21. Larsen CG, Anderson AO, Oppenheim JJ, Matsushima K. 1989. Production of interleukin-8 by human dermal fibroblasts and keratinocytes in response to interleukin-1 or tumour necrosis factor. Immunology 68: 31-36.
22. Lavker RM, Tseng SC, Sun TT. 2004. Corneal epithelial stem cells at the limbus: Looking at some old problems from a new angle. Exp Eye Res 78: 433-446.
23. Le Hir M, Hegyi I, Cueni-Loffing D, Loffing J, Kaissling B. 2005. Characterization of renal interstitial fibroblast-specific protein 1/S100A4-positive cells in healthy and inflamed rodent kidneys. Histochem Cell Biol 123: 335-346.
24. Li JH, Wang W, Huang XR, Oldfield M, Schmidt AM, Cooper ME, Lan HY. 2004. Advanced glycation end products induce tubular epithelial-myofibroblast transition through the RAGE-ERK1/2 MAP kinase signaling pathway. Am J Pathol 164: 1389-1397.
25. Li W, Hayashida Y, Chen YT, Tseng SC. 2007. Niche regulation of corneal epithelial stem cells at the limbus. Cell Res 17: 26-36.
26. Liu ZH, Striker GE, Stetler-Stevenson M, Fukushima P, Patel A, Striker LJ. 1996. TNF-alpha and IL-1 alpha induce mannose receptors and apoptosis in glomerular mesangial but not endothelial cells. Am J Physiol 270: C1595-C1601.
27. Liu S, Dontu G, Wicha MS. 2005. Mammary stem cells, self-renewal pathways, and carcinogenesis. Breast Cancer Res 7: 86-95.
28. Lucia MS, Sporn MB, Roberts AB, Stewart LV, Danielpour D. 1998. The role of transforming growth factor-beta1, -beta2, and -beta3 in androgen-responsive growth of NRP-152 rat prostatic epithelial cells. J Cell Physiol 175: 184-192.
29. Massague J, Wotton D. 2000. Transcriptional control by the TGF-beta/Smad signaling system. EMBO J 19: 1745-1754.
30. Masszi A, Di Ciano C, Sirokmany G, Arthur WT, Rotstein OD, Wang J, McCulloch CA, Rosivall L, Mucsi I, Kapus A. 2003. Central role for Rho in TGF-beta1-induced alpha-smooth muscle actin expression during epithelial-mesenchymal transition. Am J Physiol Renal Physiol 284: F911-F924.
31. Masszi A, Fan L, Rosivall L, McCulloch CA, Rotstein OD, Mucsi I, Kapus A. 2004. Integrity of cell-cell contacts is a critical regulator of TGF-beta 1-induced epithelial-to-myofibroblast transition: Role for beta-catenin. Am J Pathol 165: 1955-1967.
32. McCartney-Francis NL, Wahl SM. 1994. Transforming growth factor β: A matter of life and death. J Leukoc Biol 55: 401-409.
33. Medici D, Hay ED, Goodenough DA. 2006. Cooperation between snail and LEF-1 transcription factors is essential for TGF-beta1-induced epithelial-mesenchymal transition. Mol Biol Cell 17: 1871-1879.
34. Miettinen PJ, Ebner R, Lopez AR, Derynck R. 1994. TGF-beta induced transdifferentiation of mammary epithelial cells to mesenchymal cells: Involvement of type I receptors. J Cell Biol 127: 2021-2036.
35. Migliaccio G, Migliaccio AR, Adamson JW. 1988. In vitro differentiation of human granulocyte/macrophage and erythroid progenitors: Comparative analysis of the influence of recombinant human erythropoietin, G-CSF, GM-CSF, and IL-3 in serum-supplemented and serum-deprived cultures. Blood 72: 248-256.
36. Nagar B, Overduin M, Ikura M, Rini JM. 1996. Structural basis of calcium-induced E-cadherin rigidification and dimerization. Nature 380: 360-364.
37. Nawshad A, Hay ED. 2003. TGFbeta3 signaling activates transcription of the LEF1 gene to induce epithelial mesenchymal transformation during mouse palate development. J Cell Biol 163: 1291-1301.
38. Nelson WJ, Nusse R. 2004. Convergence of Wnt, beta-catenin, and cadherin pathways. Science 303: 1483-1487.
39. Okada H, Danoff TM, Kalluri R, Neilson EG. 1997. Early role of Fsp1 in epithelial-mesenchymal transformation. Am J Physiol 273: F563-F574.
40. Owens DW, McLean GW, Wyke AW, Paraskeva C, Parkinson EK, Frame MC, Brunton VG. 2000. The catalytic activity of the Src family kinases is required to disrupt cadherin-dependent cell-cell contacts. Mol Biol Cell 11: 51-64.
41. Reguly T, Wrana JL. 2003. In or out? The dynamics of Smad nucleocytoplasmic shuttling. Trends Cell Biol 13: 216-220.
42. Reya T, Duncan AW, Ailles L, Domen J, Scherer DC, Willert K, Hintz L, Nusse R, Weissman IL. 2003. A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature 423: 409-414.
43. Risse Marsh BC, Massaro-Giordano M, Marshall CM, Lavker RM, Jensen PJ. 2002. Initiation and characterization of keratinocyte cultures from biopsies of normal human conjunctiva. Exp Eye Res 74: 61-69.
44. Rossini M, Cheunsuchon B, Donnert E, Ma LJ, Thomas JW, Neilson EG, Fogo AB. 2005. Immunolocalization of fibroblast growth factor-1 (FGF-1), its receptor (FGFR-1), and fibroblast-specific protein-1 (FSP-1) in inflammatory renal disease. Kidney Int 68: 2621-2628.
45. Ryan DG, Taliana L, Sun L, Wei ZG, Masur SK, Lavker RM. 2003. Involvement of S100A4 in stromal fibroblasts of the regenerating cornea. Invest Ophthalmol Vis Sci 44: 4255-4262.
46. Saika S, Kono-Saika S, Ohnishi Y, Sato M, Muragaki Y, Ooshima A, Flanders KC, Yoo J, Anzano M, Liu CY, Kao WW, Roberts AB. 2004. Smad3 signaling is required for epithelial-mesenchymal transition of lens epithelium after injury. Am J Pathol 164: 651-663.
47. Savagner P. 2001. Leaving the neighborhood: Molecular mechanisms involved during epithelial-mesenchymal transition. BioEssays 23: 912-923.
48. Siegel PM, Massague J. 2003. Cytostatic and apoptotic actions of TGF-beta in homeostasis and cancer. Nat Rev Cancer 3: 807-821.
49. ten Dijke P, Hill CS. 2004. New insights into TGF-beta-Smad signalling. Trends Biochem Sci 29: 265-273.
50. Thiery JP, Sleeman JP. 2006. Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol 7: 131-142.
51. Tian YC, Fraser D, Attisano L, Phillips AO. 2003. TGF-beta1-mediated alterations of renal proximal tubular epithelial cell phenotype. Am J Physiol Renal Physiol 285: F130-F142.
52. Tseng SCG, Espana EM, Kawakita T, Di Pascuale MA, Wei Z-G, He H, Liu TS, Cho TH, Gao YY, Yeh LK, Liu C-Y. 2004. How does amniotic membrane work? The Ocular Surface 2: 177-187.
53. Willis BC, Liebler JM, Luby-Phelps K, Nicholson AG, Crandall ED, du Bois RM, Borok Z. 2005. Induction of epithelial-mesenchymal transition in alveolar epithelial cells by transforming growth factor-beta1: Potential role in idiopathic pulmonary fibrosis. Am J Pathol 166: 1321-1332.
54. Yang J, Liu Y. 2001. Dissection of key events in tubular epithelial to myofibroblast transition and its implications in renal interstitial fibrosis. Am J Pathol 159: 1465-1475.
55. Yang A, Kaghad M, Wang Y, Gillett E, Fleming MD, Dotsch V, Andrews NC, Caput D, McKeon F. 1998. p63, a p53 homolog at 3q27-29, encodes multiple products with transactivating, death-inducing, and dominant-negative activities. Mol Cell 2: 305-316.
56. Yao HW, Xie QM, Chen JQ, Deng YM, Tang HF. 2004. TGF-beta1 induces alveolar epithelial to mesenchymal transition in vitro. Life Sci 76: 29-37.
57. Yook JI, Li XY, Ota I, Fearon ER, Weiss SJ. 2005. Wnt-dependent regulation of the E-cadherin repressor snail. J Biol Chem 280: 11740-11748.
58. Yuspa SH, Hennings H, Tucker RW, Jaken S, Kilkenny AE, Roop DR. 1988. Signal transduction for proliferation and differentiation in keratinocytes. Ann NY Acad Sci 548: 191-196.
59. Zeisberg M, Bonner G, Maeshima Y, Colorado P, Muller GA, Strutz F, Kalluri R. 2001. Renal fibrosis: Collagen composition and assembly regulates epithelial-mesenchymal transdifferentiation. Am J Pathol 159: 1313-1321.