Essential role of BMPs in FGF-induced secondary lens fiber differentiation

Developmental Biology

Volumn 324, Issue 2, 2008, Pages 202-212

  Boswell, Bruce A ^a   Overbeek, Paul A ^b   Musil, Linda S ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

BMP; Differentiation; FGF; Fiber; Lens

Indexed keywords

ANTIBODY; BIOLOGICAL MARKER; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; CRYSTALLIN; FIBROBLAST GROWTH FACTOR; NOGGIN; OSTEOGENIC PROTEIN 1;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; HUMAN; LENS FIBER; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; VITREOUS BODY;

MUS MUSCULUS;

EID: 56449131346     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2008.09.003     Document Type: Article

References (71)

1. Beebe D., Garcia C., Wang X., Rajagopal R., Feldmeier M., Kim J.Y., Chytil A., Moses H., Ashery-Padan R., and Rauchman M. Contributions by members of the TGFbeta superfamily to lens development. Int. J. Dev. Biol. 48 (2004) 845-856
2. Belecky-Adams T.L., Adler R., and Beebe D.C. Bone morphogenetic protein signaling and the initiation of lens fiber cell differentiation. Development 129 (2002) 3795-3802
3. Bowers R.R., Kim J.W., Otto T.C., and Lane M.D. Stable stem cell commitment to the adipocyte lineage by inhibition of DNA methylation: role of the BMP-4 gene. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 13022-13027
4. Caruelle D., Groux-Muscatelli B., Gaudric A., Sestier C., Coscas G., Caruelle J.P., and Barritault D. Immunological study of acidic fibroblast growth factor (aFGF) distribution in the eye. J. Cell. Biochem. 39 (1989) 117-128
5. Chow R.L., Roux G.D., Roghani M., Palmer M.A., Rifkin D.B., Moscatelli D.A., and Lang R.A. FGF suppresses apoptosis and induces differentiation of fibre cells in the mouse lens. Development 121 (1995) 4383-4393
6. Coulombre J.L., and Coulombre A.J. Lens elongation: fiber elongation and lens orientation. Science 142 (1963) 1489-1490
7. David L.L., Dickey B.M., and Shearer T.R. Origin of urea-soluble protein in the selenite cataract. Role of beta-crystallin proteolysis and calpain II. Invest. Ophthalmol. Vis. Sci. 28 (1987) 1148-1156
8. Dawes L.J., Elliott R.M., Reddan J.R., Wormstone Y.M., and Wormstone I.M. Oligonucleotide microarray analysis of human lens epithelial cells: TGFbeta regulated gene expression. Mol. Vis. 13 (2007) 1181-1197
9. de Iongh R.U., Chen Y., Kokkinos M.I., and McAvoy J.W. BMP and activin receptor expression in lens development. Mol. Vis. 10 (2004) 566-576
10. DePianto D.J., Hess J.F., Blankenship T.N., and FitzGerald P.G. Isolation and characterization of the human CP49 gene promoter. Invest. Ophthalmol. Vis. Sci. 44 (2003) 235-243
11. Faber S.C., Dimanlig P., Makarenkova H.P., Shirke S., Ko K., and Lang R.A. Fgf receptor signaling plays a role in lens induction. Development 128 (2001) 4425-4438
12. Faber S.C., Robinson M.L., Makarenkova H.P., and Lang R.A. Bmp signaling is required for development of primary lens fiber cells. Development 129 (2002) 3727-3737
13. FitzGerald P.G., and Goodenough D.A. Rat lens cultures: MIP expression and domains of intercellular coupling. Invest. Ophthalmol. Vis. Sci. 27 (1986) 755-771
14. Furuta Y., and Hogan B.L. BMP4 is essential for lens induction in the mouse embryo. Genes Dev. 12 (1998) 3764-3775
15. Gerido D.A., Sellitto C., Li L., and White T.W. Genetic background influences cataractogenesis, but not lens growth deficiency, in Cx50-knockout mice. Invest. Ophthalmol. Vis. Sci. 44 (2003) 2669-2674
16. Govindarajan V., and Overbeek P.A. Secreted FGFR3, but not FGFR1, inhibits lens fiber differentiation. Development 128 (2001) 1617-1627
17. Groppe J., Greenwald J., Wiater E., Rodriguez-Leon J., Economides A.N., Kwiatkowski W., Affolter M., Vale W.W., Belmonte J.C., and Choe S. Structural basis of BMP signalling inhibition by the cystine knot protein Noggin. Nature 420 (2002) 636-642
18. Haynes T., Gutierrez C., Aycinena J.C., Tsonis P.A., and Del Rio-Tsonis K. BMP signaling mediates stem/progenitor cell-induced retina regeneration. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 20380-20385
19. Hoffmann A., Czichos S., Kaps C., Bachner D., Mayer H., Kurkalli B.G., Zilberman Y., Turgeman G., Pelled G., Gross G., and Gazit D. The T-box transcription factor Brachyury mediates cartilage development in mesenchymal stem cell line C3H10T1/2. J. Cell. Sci. 115 (2002) 769-781
20. Huang J.X., Feldmeier M., Shui Y.B., and Beebe D.C. Evaluation of fibroblast growth factor signaling during lens fiber cell differentiation. Invest. Ophthalmol. Vis. Sci. 44 (2003) 680-690
21. Hung F.C., Zhao S., Chen Q., and Overbeek P.A. Retinal ablation and altered lens differentiation induced by ocular overexpression of BMP7. Vision Res. 42 (2002) 427-438
22. Inagaki M., Irie K., Ishizaki H., Tanaka-Okamoto M., Morimoto K., Inoue E., Ohtsuka T., Miyoshi J., and Takai Y. Roles of cell-adhesion molecules nectin 1 and nectin 3 in ciliary body development. Development 132 (2005) 1525-1537
23. Ireland M.E., Goebel D.J., Maisel H., Kiner D., and Poosch M.S. Quantification and regulation of mRNAs encoding beaded filament proteins in the chick lens. Curr. Eye Res. 16 (1997) 838-846
24. Ishizaki Y., Voyvodic J.T., Burne J.F., and Raff M.C. Control of lens epithelial cell survival. J. Cell. Biol. 121 (1993) 899-908
25. Le A.C., and Musil L.S. Normal differentiation of cultured lens cells after inhibition of gap junction-mediated intercellular communication. Dev. Biol. 204 (1998) 80-96
26. Le A.-C.N., and Musil L.S. FGF signaling in chick lens development. Dev. Biol. 233 (2001) 394-411
27. Le A.C., and Musil L.S. A novel role for FGF and extracellular signal-regulated kinase in gap junction-mediated intercellular communication in the lens. J. Cell. Biol. 154 (2001) 197-216
28. Lein P.J., Beck H.N., Chandrasekaran V., Gallagher P.J., Chen H.L., Lin Y., Guo X., Kaplan P.L., Tiedge H., and Higgins D. Glia induce dendritic growth in cultured sympathetic neurons by modulating the balance between bone morphogenetic proteins (BMPs) and BMP antagonists. J. Neurosci. 22 (2002) 10377-10387
29. Li X., Schwarz E.M., Zuscik M.J., Rosier R.N., Ionescu A.M., Puzas J.E., Drissi H., Sheu T.J., and O'Keefe R.J. Retinoic acid stimulates chondrocyte differentiation and enhances bone morphogenetic protein effects through induction of Smad1 and Smad5. Endocrinology 144 (2003) 2514-2523
30. Lovicu F.J., and McAvoy J.W. The age of rats affects the response of lens epithelial explants to fibroblast growth factor. An ultrastructural analysis. Invest. Ophthalmol. Vis. Sci. 33 (1992) 2269-2278
31. Lovicu F.J., and McAvoy J.W. Localization of acidic fibroblast growth factor, basic fibroblast growth factor, and heparan sulphate proteoglycan in rat lens: implications for lens polarity and growth patterns. Invest. Ophthalmol. Vis. Sci. 34 (1993) 3355-3365
32. Lovicu F.J., and McAvoy J.W. FGF-induced lens cell proliferation and differentiation is dependent on MAPK (ERK1/2) signalling. Development 128 (2001) 5075-5084
33. Lovicu F.J., and McAvoy J.W. Growth factor regulation of lens development. Dev. Biol. 280 (2005) 1-14
34. Lovicu F.J., and Overbeek P.A. Overlapping effects of different members of the FGF family on lens fiber differentiation in transgenic mice. Development 125 (1998) 3365-3377
35. Lovicu F.J., de Iongh R.U., and McAvoy J.W. Expression of FGF-1 and FGF-2 mRNA during lens morphogenesis, differentiation and growth. Curr. Eye Res. 16 (1997) 222-230
36. Massague J. TGF-beta signal transduction. Annu. Rev. Biochem. 67 (1998) 753-791
37. McAvoy J.W., and Chamberlain C.G. Fibroblast growth factor (FGF) induces different responses in lens epithelial cells depending on its concentration. Development 107 (1989) 221-228
38. Menko A. Lens epithelial cell differentiation. Exp. Eye Res. 75 (2002) 485-490
39. Menko A.S., Klukas K.A., and Johnson R.G. Chicken embryo lens cultures mimic differentiation in the lens. Dev. Biol. 103 (1984) 129-141
40. Menko A.S., Klukas K.A., Liu T.F., Quade B., Sas D.F., Preus D.M., and Johnson R.G. Junctions between lens cells in differentiating cultures: structure, formation, intercellular permeability, and junctional protein expression. Dev. Biol. 123 (1987) 307-320
41. Mohammadi M., Froum S., Hamby J.M., Schroeder M.C., Panek R.L., Lu G.H., Eliseenkova A.V., Green D., Schlessinger J., and Hubbard S.R. Crystal structure of an angiogenesis inhibitor bound to the FGF receptor tyrosine kinase domain. EMBO J. 17 (1998) 5896-5904
42. Montero J.A., Ganan Y., Macias D., Rodriguez-Leon J., Sanz-Ezquerro J.J., Merino R., Chimal-Monroy J., Nieto M.A., and Hurle J.M. Role of FGFs in the control of programmed cell death during limb development. Development 128 (2001) 2075-2084
43. Okada T.S., Eguchi G., and Takeichi M. The expression of differentiation by chicken lens epithelium in in vitro cell culture. Dev. Growth Differ. 13 (1971) 323-336
44. Piatigorsky J. Intracellular ions, protein metabolism, and cataract formation. Curr. Top. Eye Res. 3 (1980) 1-39
45. Piatigorsky J. Lens differentiation in vertebrates. A review of cellular and molecular features. Differentiation 19 (1981) 134-153
46. Piatigorsky J., Webster H.D., and Craig S.P. Protein synthesis and ultrastructure during the formation of embryonic chick lens fibers in vivo and in vitro. Dev. Biol. 27 (1972) 176-189
47. Quinlan R.A., Carter J.M., Sandilands A., and Prescott A.R. The beaded filament of the eye lens: an unexpected key to intermediate filament structure and function. Trends Cell Biol. 6 (1996) 123-126
48. Rajagopal R., Ishii S., and Beebe D.C. Intracellular mediators of transforming growth factor beta superfamily signaling localize to endosomes in chicken embryo and mouse lenses in vivo. BMC Cell. Biol. 8 (2007) 25
49. Renaud F., Oliver L., Desset S., Tassin J., Romquin N., Courtois Y., and Laurent M. Up-regulation of aFGF expression in quiescent cells is related to cell survival. J. Cell. Physiol. 158 (1994) 435-443
50. Richardson N.A., McAvoy J.W., and Chamberlain C.G. Age of rats affects response of lens epithelial explants to fibroblast growth factor. Exp. Eye Res. 55 (1992) 649-656
51. Richardson N.A., Chamberlain C.G., and McAvoy J.W. IGF-1 enhancement of FGF-induced lens fiber differentiation in rats of different ages. Invest. Ophthalmol. Vis. Sci. 34 (1993) 3303-3312
52. Robinson M.L. An essential role for FGF receptor signaling in lens development. Semin. Cell Dev. Biol. 17 (2006) 726-740
53. Robinson M.L., MacMillan-Crow L.A., Thompson J.A., and Overbeek P.A. Expression of a truncated FGF receptor results in defective lens development in transgenic mice. Development 121 (1995) 3959-3967
54. Robinson M.L., Overbeek P.A., Verran D.J., Grizzle W.E., Stockard C.R., Friesel R., Maciag T., and Thompson J.A. Extracellular FGF-1 acts as a lens differentiation factor in transgenic mice. Development 121 (1995) 505-514
55. Robinson M.L., Ohtaka-Maruyama C., Chan C.C., Jamieson S., Dickson C., Overbeek P.A., and Chepelinsky A.B. Disregulation of ocular morphogenesis by lens-specific expression of FGF-3/int-2 in transgenic mice. Dev. Biol. 198 (1998) 13-31
56. Rossi J.M., Dunn N.R., Hogan B.L., and Zaret K.S. Distinct mesodermal signals, including BMPs from the septum transversum mesenchyme, are required in combination for hepatogenesis from the endoderm. Genes Dev. 15 (2001) 1998-2009
57. Schulz M.W., Chamberlain C.G., de Iongh R.U., and McAvoy J.W. Acidic and basic FGF in ocular media and lens: implications for lens polarity and growth patterns. Development 118 (1993) 117-126
58. Schweigerer L., Ferrara N., Haaparanta T., Neufeld G., and Gospodarowicz D. Basic fibroblast growth factor: expression in cultured cells derived from corneal endothelium and lens epithelium. Exp. Eye Res. 46 (1988) 71-80
59. Shou J., Murray R.C., Rim P.C., and Calof A.L. Opposing effects of bone morphogenetic proteins on neuron production and survival in the olfactory receptor neuron lineage. Development 127 (2000) 5403-5413
60. Simirskii V.N., Lee R.S., Wawrousek E.F., and Duncan M.K. Inbred FVB/N mice are mutant at the cp49/Bfsp2 locus and lack beaded filament proteins in the lens. Invest. Ophthalmol. Vis. Sci. 47 (2006) 4931-4934
61. Stolen C.M., and Griep A.E. Disruption of lens fiber cell differentiation and survival at multiple stages by region-specific expression of truncated FGF receptors. Dev. Biol. 217 (2000) 205-220
62. Stump R.J., Lovicu F.J., Ang S.L., Pandey S.K., and McAvoy J.W. Lithium stabilizes the polarized lens epithelial phenotype and inhibits proliferation, migration, and epithelial mesenchymal transition. J. Pathol. 210 (2006) 249-257
63. Tholozan F.M., Gribbon C., Li Z., Goldberg M.W., Prescott A.R., McKie N., and Quinlan R.A. FGF-2 release from the lens capsule by MMP-2 maintains lens epithelial cell viability. Mol. Biol. Cell. 18 (2007) 4222-4231
64. Thut C.J., Rountree R.B., Hwa M., and Kingsley D.M. A large-scale in situ screen provides molecular evidence for the induction of eye anterior segment structures by the developing lens. Dev. Biol. 231 (2001) 63-76
65. Vinader L.M., van Genesen S.T., de Jong W.W., and Lubsen N.H. Influence of hormones and growth factors on lens protein composition: the effect of dexamethasone and PDGF-AA. Mol. Vis. 9 (2003) 723-729
66. Vukicevic S., Latin V., Chen P., Batorsky R., Reddi A.H., and Sampath T.K. Localization of osteogenic protein-1 (bone morphogenetic protein-7) during human embryonic development: high affinity binding to basement membranes. Biochem. Biophys. Res. Commun. 198 (1994) 693-700
67. Wawersik S., Purcell P., Rauchman M., Dudley A.T., Robertson E.J., and Maas R. BMP7 acts in murine lens placode development. Dev. Biol. 207 (1999) 176-188
68. Yamamoto Y. Growth of lens and ocular environment: role of neural retina in the growth of mouse lens as revealed by an implantation experiment. Dev. Growth Differ. 18 (1976) 273-278
69. Zhao S., Chen Q., Hung F.C., and Overbeek P.A. BMP signaling is required for development of the ciliary body. Development 129 (2002) 4435-4442
70. Zhao H., Yang T., Madakashira B.P., Thiels C.A., Bechtle C.A., Garcia C.M., Zhang H., Yu K., Ornitz D.M., Beebe D.C., and Robinson M.L. Fibroblast growth factor receptor signaling is essential for lens fiber cell differentiation. Dev. Biol. 318 (2008) 276-288
71. Zimmerman L.B., De Jesus-Escobar J.M., and Harland R.M. The Spemann organizer signal noggin binds and inactivates bone morphogenetic protein 4. Cell 86 (1996) 599-606