Synergistic interaction between the fibroblast growth factor and bone morphogenetic protein signaling pathways in lens cells

Molecular Biology of the Cell

Volumn 26, Issue 13, 2015, Pages 2561-2572

  Boswell, Bruce A ^a   Musil, Linda S ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 4; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR 9; FIBROBLAST GROWTH FACTOR RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; NOGGIN; TRANSFORMING GROWTH FACTOR BETA1; CRYSTALLIN; RECOMBINANT PROTEIN;

ANIMAL CELL; ARTICLE; CELL COMMUNICATION; CELL DIFFERENTIATION; CHICK; CONTROLLED STUDY; GAP JUNCTION; GENE EXPRESSION REGULATION; INTRACELLULAR SIGNALING; LENS EPITHELIUM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; UPREGULATION; ANIMAL; BOVINE; CELL CULTURE; CHICK EMBRYO; EPITHELIUM CELL; GROWTH, DEVELOPMENT AND AGING; HUMAN; LENS; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; BONE MORPHOGENETIC PROTEINS; CATTLE; CELL COMMUNICATION; CELL DIFFERENTIATION; CELLS, CULTURED; CHICK EMBRYO; CRYSTALLINS; EPITHELIAL CELLS; FIBROBLAST GROWTH FACTORS; GAP JUNCTIONS; HUMANS; LENS, CRYSTALLINE; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION;

EID: 84934299864     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E15-02-0117     Document Type: Article

References (102)

1. Bakrania P, Efthymiou M, Klein JC, Salt A, Bunyan DJ, Wyatt A, Ponting CP, Martin A, Williams S, Lindley V, et al. (2008). Mutations in BMP4 cause eye, brain, and digit developmental anomalies: overlap between the BMP4 and hedgehog signaling pathways. Am J Hum Genet 82, 304-319.
2. Baldo GJ, Mathias RT (1992). Spatial variations in membrane properties in the intact rat lens. Biophys J 63, 518-529.
3. Beebe D, Garcia C, Wang X, Rajagopal R, Feldmeier M, Kim JY, Chytil A, Moses H, Ashery-Padan R, Rauchman M (2004). Contributions by members of the TGFbeta superfamily to lens development. Int J Dev Biol 48, 845-856.
4. Boswell BA, Le AC, Musil LS (2009). Upregulation and maintenance of gap junctional communication in lens cells. Exp Eye Res 88, 919-927.
5. Boswell BA, Lein PJ, Musil LS (2008a). Cross-talk between fibroblast growth factor and bone morphogenetic proteins regulates gap junction-mediated intercellular communication in lens cells. Mol Biol Cell 19, 2631-2641.
6. Boswell BA, Overbeek PA, Musil LS (2008b). Essential role of BMPs in FGF-induced secondary lens fiber differentiation. Dev Biol 324, 202-212.
7. Chen P, Kroog GS (2004). Alterations in receptor expression or agonist concentration change the pathways gastrin-releasing peptide receptor uses to regulate extracellular signal-regulated kinase. Mol Pharmacol 66, 1625-1634.
8. Cho JY, Guo C, Torello M, Lunstrum GP, Iwata T, Deng C, Horton WA (2004). Defective lysosomal targeting of activated fibroblast growth factor receptor 3 in achondroplasia. Proc Natl Acad Sci USA 101, 609-614.
9. Dawes LJ, Elliott RM, Reddan JR, Wormstone YM, Wormstone IM (2007). Oligonucleotide microarray analysis of human lens epithelial cells: TGFbeta regulated gene expression. Mol Vis 13, 1181-1197.
10. de Iongh RU, Chen Y, Kokkinos MI, McAvoy JW (2004). BMP and activin receptor expression in lens development. Mol Vis 10, 566-576.
11. Dias da Silva MR, Tiffin N, Mima T, Mikawa T, Hyer J (2007). FGF-mediated induction of ciliary body tissue in the chick eye. Dev Biol 304, 272-285.
12. Donaldson P, Kistler J, Mathias RT (2001). Molecular solutions to mammalian lens transparency. News Physiol Sci 16, 118-123.
13. Du Y, Xiao Q, Yip HK (2010). Regulation of retinal progenitor cell differentiation by bone morphogenetic protein 4 is mediated by the smad/id cascade. Invest Ophthalmol Vis Sci 51, 3764-3773.
14. Dudley AT, Godin RE, Robertson EJ (1999). Interaction between FGF and BMP signaling pathways regulates development of metanephric mesenchyme. Genes Dev 13, 1601-1613.
15. Eswarakumar VP, Lax I, Schlessinger J (2005). Cellular signaling by fibroblast growth factor receptors. Cytokine Growth Factor Rev 16, 139-149.
16. Faber SC, Dimanlig P, Makarenkova HP, Shirke S, Ko K, Lang RA (2001). Fgf receptor signaling plays a role in lens induction. Development 128, 4425-4438.
17. Furuta Y, Hogan BL (1998). BMP4 is essential for lens induction in the mouse embryo. Genes Dev 12, 3764-3775.
18. Govindarajan V, Overbeek PA (2001). Secreted FGFR3, but not FGFR1, inhibits lens fiber differentiation. Development 128, 1617-1627.
19. Groppe J, Greenwald J, Wiater E, Rodriguez-Leon J, Economides AN, Kwiatkowski W, Affolter M, Vale WW, Belmonte JC, Choe S (2002). Structural basis of BMP signalling inhibition by the cystine knot protein Noggin. Nature 420, 636-642.
20. Hollnagel A, Oehlmann V, Heymer J, Ruther U, Nordheim A (1999). Id genes are direct targets of bone morphogenetic protein induction in embryonic stem cells. J Biol Chem 274, 19838-19845.
21. Hung FC, Zhao S, Chen Q, Overbeek PA (2002). Retinal ablation and altered lens differentiation induced by ocular overexpression of BMP7. Vision Res 42, 427-438.
22. Isaac A, Cohn MJ, Ashby P, Ataliotis P, Spicer DB, Cooke J, Tickle C (2000). FGF and genes encoding transcription factors in early limb specification. Mech Dev 93, 41-48.
23. Jarrin M, Pandit T, Gunhaga L (2012). A balance of FGF and BMP signals regulates cell cycle exit and Equarin expression in lens cells. Mol Biol Cell 23, 3266-3274.
24. Kamaid A, Neves J, Giraldez F (2010). Id gene regulation and function in the prosensory domains of the chicken inner ear: a link between Bmp signaling and Atoh1. J Neurosci 30, 11426-11434.
25. Katagiri T, Imada M, Yanai T, Suda T, Takahashi N, Kamijo R (2002). Identification of a BMP-responsive element in Id1, the gene for inhibition of myogenesis. Genes Cells 7, 949-960.
26. Knights V, Cook SJ (2010). De-regulated FGF receptors as therapeutic targets in cancer. Pharmacol Ther 125, 105-117.
27. Kolch W, Heidecker G, Kochs G, Hummel R, Vahidi H, Mischak H, Finkenzeller G, Marme D, Rapp UR (1993). Protein kinase C alpha activates RAF-1 by direct phosphorylation. Nature 364, 249-252.
28. Korchynskyi O, ten Dijke P (2002). Identification and functional characterization of distinct critically important bone morphogenetic protein-specific response elements in the Id1 promoter. J Biol Chem 277, 4883-4891.
29. Kovalenko D, Yang X, Nadeau RJ, Harkins LK, Friesel R (2003). Sef inhibits fibroblast growth factor signaling by inhibiting FGFR1 tyrosine phosphorylation and subsequent ERK activation. J Biol Chem 278, 14087-14091.
30. Kozmikova I, Candiani S, Fabian P, Gurska D, Kozmik Z (2013). Essential role of Bmp signaling and its positive feedback loop in the early cell fate evolution of chordates. Dev Biol 382, 538-554.
31. Kretzschmar M, Doody J, Massague J (1997). Opposing BMP and EGF signalling pathways converge on the TGF-beta family mediator Smad1. Nature 389, 618-622.
32. Le AC, Musil LS (1998). Normal differentiation of cultured lens cells after inhibition of gap junction-mediated intercellular communication. Dev Biol 204, 80-96.
33. Le AC, Musil LS (2001a). FGF signaling in chick lens development. Dev Biol 233, 394-411.
34. Le AC, Musil LS (2001b). A novel role for FGF and extracellular signal-regulated kinase in gap junction-mediated intercellular communication in the lens. J Cell Biol 154, 197-216.
35. Li H, Tao C, Cai Z, Hertzler-Schaefer K, Collins TN, Wang F, Feng GS, Gotoh N, Zhang X (2014). Frs2a and Shp2 signal independently of Gab to mediate FGF signaling in lens development. J Cell Sci 127, 571-582.
36. Li P, Oparil S, Sun JZ, Thompson JA, Chen YF (2003). Fibroblast growth factor mediates hypoxia-induced endothelin - a receptor expression in lung artery smooth muscle cells. J Appl Physiol 95, 643-651.
37. Logeart-Avramoglou D, Bourguignon M, Oudina K, Ten Dijke P, Petite H (2006). An assay for the determination of biologically active bone morphogenetic proteins using cells transfected with an inhibitor of differentiation promoter-luciferase construct. Anal Biochem 349, 78-86.
38. Lopez-Rovira T, Chalaux E, Massague J, Rosa JL, Ventura F (2002). Direct binding of Smad1 and Smad4 to two distinct motifs mediates bone morphogenetic protein-specific transcriptional activation of Id1 gene. J Biol Chem 277, 3176-3185.
39. Lovicu FJ, McAvoy JW (2001). FGF-induced lens cell proliferation and differentiation is dependent on MAPK (ERK1/2) signalling. Development 128, 5075-5084.
40. Lovicu FJ, McAvoy JW (2005). Growth factor regulation of lens development. Dev Biol 280, 1-14.
41. Lovicu FJ, McAvoy JW, de Iongh RU (2011). Understanding the role of growth factors in embryonic development: insights from the lens. Philos Trans R Soc Lond B Biol Sci 366, 1204-1218.
42. Lovicu FJ, Overbeek PA (1998). Overlapping effects of different members of the FGF family on lens fiber differentiation in transgenic mice. Development 125, 3365-3377.
43. Madakashira BP, Kobrinski DA, Hancher AD, Arneman EC, Wagner BD, Wang F, Shin H, Lovicu FJ, Reneker LW, Robinson ML (2012). Frs2a enhances fibroblast growth factor-mediated survival and differentiation in lens development. Development 139, 4601-4612.
44. Maier E, von Hofsten J, Nord H, Fernandes M, Paek H, Hébert JM, Gunhaga L (2010). Opposing Fgf and Bmp activities regulate the specification of olfactory sensory and respiratory epithelial cell fates. Development 137, 1601-1611.
45. Massague J (2003). Integration of Smad and MAPK pathways: a link and a linker revisited. Genes Dev 17, 2993-2997.
46. Mathias RT, Rae JL, Baldo GJ (1997). Physiological properties of the normal lens. Physiol Rev 77, 21-50.
47. McAvoy JW, Chamberlain CG (1989). Fibroblast growth factor (FGF) induces different responses in lens epithelial cells depending on its concentration. Development 107, 221-228.
48. McAvoy JW, Chamberlain CG, de Iongh RU, Hales AM, Lovicu FJ (1999). Lens development. Eye 13, 425-437.
49. Menko AS, Klukas KA, Johnson RG (1984). Chicken embryo lens cultures mimic differentiation in the lens. Dev Biol 103, 129-141.
50. Mochizuki T, Masai I (2014). The lens equator: a platform for molecular machinery that regulates the switch from cell proliferation to differentiation in the vertebrate lens. Dev Growth Differ 56, 387-401.
51. Monteiro RM, de Sousa Lopes SM, Korchynskyi O, ten Dijke P, Mummery CL (2004). Spatio-temporal activation of Smad1 and Smad5 in vivo: monitoring transcriptional activity of Smad proteins. J Cell Sci 117, 4653-4663.
52. Musil LS (2012). Primary cultures of embryonic chick lens cells as a model system to study lens gap junctions and fiber cell differentiation. J Membr Biol 245, 357-368.
53. Nehlin JO, Hara E, Kuo WL, Collins C, Campisi J (1997). Genomic organization, sequence, and chromosomal localization of the human helix-loop-helix Id1 gene. Biochem Biophys Res Commun 231, 628-634.
54. Nishiguchi S, Wood H, Kondoh H, Lovell-Badge R, Episkopou V (1998). Sox1 directly regulates the gamma-crystallin genes and is essential for lens development in mice. Genes Dev 12, 776-781.
55. Niswander L, Martin GR (1993). FGF-4 and BMP-2 have opposite effects on limb growth. Nature 361, 68-71.
56. Obata H, Kaji Y, Yamada H, Kato M, Tsuru T, Yamashita H (1999). Expression of transforming growth factor-beta superfamily receptors in rat eyes. Acta Ophthalmol Scand 77, 151-156.
57. Pan Y, Woodbury A, Esko JD, Grobe K, Zhang X (2006). Heparan sulfate biosynthetic gene Ndst1 is required for FGF signaling in early lens development. Development 133, 4933-4944.
58. Piatigorsky J (1981). Lens differentiation in vertebrates. A review of cellular and molecular features. Differentiation 19, 134-153.
59. Rajagopal R, Huang J, Dattilo LK, Kaartinen V, Mishina Y, Deng CX, Umans L, Zwijsen A, Roberts AB, Beebe DC (2009). The type I BMP receptors, Bmpr1a and Acvr1, activate multiple signaling pathways to regulate lens formation. Dev Biol 335, 305-316.
60. Rajagopal R, Ishii S, Beebe DC (2007). Intracellular mediators of transforming growth factor beta superfamily signaling localize to endosomes in chicken embryo and mouse lenses in vivo. BMC Cell Biol 8, 25.
61. Reinhold MI, Abe M, Kapadia RM, Liao Z, Naski MC (2004). FGF18 represses noggin expression and is induced by calcineurin. J Biol Chem 279, 38209-38219.
62. Reneker LW, Overbeek PA (1996). Lens-specific expression of PDGF-A alters lens growth and development. Dev Biol 180, 554-565.
63. Reuss B, von Bohlen und Halbach O (2003). Fibroblast growth factors and their receptors in the central nervous system. Cell Tissue Res 313, 139-157.
64. Rice R, Thesleff I, Rice DP (2005). Regulation of Twist, Snail, and Id1 is conserved between the developing murine palate and tooth. Dev Dynam 234, 28-35.
65. Richardson NA, Chamberlain CG, McAvoy JW (1993). IGF-1 enhancement of FGF-induced lens fiber differentiation in rats of different ages. Invest Ophthalmol Vis Sci 34, 3303-3312.
66. Richardson NA, McAvoy JW, Chamberlain CG (1992). Age of rats affects response of lens epithelial explants to fibroblast growth factor. Exp Eye Res 55, 649-656.
67. Robinson ML (2006). An essential role for FGF receptor signaling in lens development. Semin Cell Dev Biol 17, 726-740.
68. Rozenblatt-Rosen O, Mosonego-Ornan E, Sadot E, Madar-Shapiro L, Sheinin Y, Ginsberg D, Yayon A (2002). Induction of chondrocyte growth arrest by FGF: transcriptional and cytoskeletal alterations. J Cell Sci 115, 553-562.
69. Sapkota G, Alarcon C, Spagnoli FM, Brivanlou AH, Massague J (2007). Balancing BMP signaling through integrated inputs into the Smad1 linker. Mol Cell 25, 441-454.
70. Satow R, Kurisaki A, Chan TC, Hamazaki TS, Asashima M (2006). Dullard promotes degradation and dephosphorylation of BMP receptors and is required for neural induction. Dev Cell 11, 763-774.
71. Schuler-Metz A, Knöchel S, Kaufmann E, Knöchel W (2000). The homeodomain transcription factor Xvent-2 mediates autocatalytic regulation of BMP-4expression in Xenopus embryos. J Biol Chem 275, 34365-34374.
72. Schulz MW, Chamberlain CG, de Iongh RU, McAvoy JW (1993). Acidic and basic FGF in ocular media and lens: implications for lens polarity and growth patterns. Development 118, 117-126.
73. Shin M, Ohte S, Fukuda T, Sasanuma H, Yoneyama K, Kokabu S, Miyamoto A, Tsukamoto S, Hohjoh H, Jimi E, Katagiri T (2013). Identification of a novel bone morphogenetic protein (BMP) inducible transcript, BMP-inducible transcript-1, by utilizing the conserved BMP-responsive elements in the Id genes. J Bone Miner Metab 31, 34-43.
74. Sjödal M, Edlund T, Gunhaga L (2007). Time of exposure to BMP signals plays a key role in the specification of the olfactory and lens placodes ex vivo. Dev Cell 13, 141-149.
75. Song K, Krause C, Shi S, Patterson M, Suto R, Grgurevic L, Vukicevic S, van Dinther M, Falb D, Ten Dijke P, Alaoui-Ismaili MH (2010). Identification of a key residue mediating bone morphogenetic protein (BMP)-6 resistance to noggin inhibition allows for engineered BMPs with superior agonist activity. J Biol Chem 285, 12169-12180.
76. Sweeney MH, Garland DL, Truscott RJ (2003). Movement of cysteine in intact monkey lenses: the major site of entry is the germinative region. Exp Eye Res 77, 245-251.
77. ten Dijke P, Korchynskyi O, Valdimarsdottir G, Goumans MJ (2003). Controlling cell fate by bone morphogenetic protein receptors. Mol Cell Endocrinol 211, 105-113.
78. Thut CJ, Rountree RB, Hwa M, Kingsley DM (2001). A large-scale in situ screen provides molecular evidence for the induction of eye anterior segment structures by the developing lens. Dev Biol 231, 63-76.
79. Tournay O, Benezra R (1996). Transcription of the dominant-negative helix-loop-helix protein Id1 is regulated by a protein complex containing the immediate-early response gene Egr-1. Mol Cell Biol 16, 2418-2430.
80. Ueda Y, Hirai S, Osada S, Suzuki A, Mizuno K, Ohno S (1996). Protein kinase C activates the MEK-ERK pathway in a manner independent of Ras and dependent on Raf. J Biol Chem 271, 23512-23519.
81. Vargas MR, Pehar M, Cassina P, Martínez-Palma L, Thompson JA, Beckman JS, Barbeito L (2005). Fibroblast growth factor-1 induces heme oxygenase-1 via nuclear factor erythroid 2-related factor 2 (Nrf2) in spinal cord astrocytes: consequences for motor neuron survival. J Biol Chem 280, 25571-25579.
82. Walshe J, Mason I (2000). Expression of FGFR1, FGFR2 and FGFR3 during early neural development in the chick embryo. Mech Dev 90, 103-110.
83. Wang Z, Weitzmann MN, Sangadala S, Hutton WC, Yoon ST (2013). Link protein N-terminal peptide binds to bone morphogenetic protein (BMP) type II receptor and drives matrix protein expression in rabbit intervertebral disc cells. J Biol Chem 288, 28243-28253.
84. Warren SM, Brunet LJ, Harland RM, Economides AN, Longaker MT (2003). The BMP antagonist noggin regulates cranial suture fusion. Nature 422, 625-629.
85. Wawersik S, Purcell P, Rauchman M, Dudley AT, Robertson EJ, Maas R (1999). BMP7 acts in murine lens placode development. Dev Biol 207, 176-188.
86. Weaver M, Dunn NR, Hogan BL (2000). Bmp4 and Fgf10 play opposing roles during lung bud morphogenesis. Development 127, 2695-2704.
87. Whitman M (1998). Smads and early developmental signaling by the TGF-beta superfamily. Genes Dev 12, 2445-2462.
88. Wijgerde M, Karp S, McMahon J, McMahon AP (2005). Noggin antagonism of BMP4 signaling controls development of the axial skeleton in the mouse. Dev Biol 286, 149-157.
89. Wilson I, Edlund T (2001). Neural induction: toward a unifying mechanism. Nat Neurosci 4, 1161-1168.
90. Wolf L, Gao CS, Gueta K, Xie Q, Chevallier T, Podduturi NR, Sun J, Conte I, Zelenka PS, Ashery-Padan R, et al. (2013). Identification and characterization of FGF2-dependent mRNA: microRNA networks during lens fiber cell differentiation. G3 (Bethesda) 3, 2239-2255.
91. Wong A, Lamothe B, Lee A, Schlessinger J, Lax I (2002). FRS2 alpha attenuates FGF receptor signaling by Grb2-mediated recruitment of the ubiquitin ligase Cbl. Proc Natl Acad Sci USA 99, 6684-6689.
92. Xian W, Schwertfeger KL, Rosen JM (2007). Distinct roles of fibroblast growth factor receptor 1 and 2 in regulating cell survival and epithelial-mesenchymal transition. Mol Endocrinol 21, 987-1000.
93. Xu N, Brodin P, Wei T, Meisgen F, Eidsmo L, Nagy N, Kemeny L, Ståhle M, Sonkoly E, Pivarcsi A (2011). MiR-125b, a microRNA downregulated in psoriasis, modulates keratinocyte proliferation by targeting FGFR2. J Invest Dermatol 131, 1521-1529.
94. Xu RH, Peck RM, Li DS, Feng X, Ludwig T, Thomson JA (2005). Basic FGF and suppression of BMP signaling sustain undifferentiated proliferation of human ES cells. Nat Methods 2, 185-190.
95. Yang Y, Stopka T, Golestaneh N, Wang Y, Wu K, Li A, Chauhan BK, Gao CY, Cveklova K, Duncan MK, et al. (2006). Regulation of alphaA-crystallin via Pax6, c-Maf, CREB and a broad domain of lens-specific chromatin. EMBO J 25, 2107-2118.
96. Yoon BS, Pogue R, Ovchinnikov DA, Yoshii I, Mishina Y, Behringer RR, Lyons KM (2006). BMPs regulate multiple aspects of growth-plate chondrogenesis through opposing actions on FGF pathways. Development 133, 4667-4678.
97. Yu PB, Hong CC, Sachidanandan C, Babitt JL, Deng DY, Hoyng SA, Lin HY, Bloch KD, Peterson RT (2008). Dorsomorphin inhibits BMP signals required for embryogenesis and iron metabolism. Nat Chem Biol 4, 33-41.
98. Zawel L, Dai JL, Buckhaults P, Zhou S, Kinzler KW, Vogelstein B, Kern SE (1998). Human Smad3 and Smad4 are sequence-specific transcription activators. Mol Cell 1, 611-617.
99. Zhao S, Chen Q, Hung FC, Overbeek PA (2002). BMP signaling is required for development of the ciliary body. Development 129, 4435-4442.
100. Zhao H, Yang T, Madakashira BP, Thiels CA, Bechtle CA, Garcia CM, Zhang H, Yu K, Ornitz DM, Beebe DC, Robinson ML (2008). Fibroblast growth factor receptor signaling is essential for lens fiber cell differentiation. Dev Biol 318, 276-288.
101. Zilberberg L, ten Dijke P, Sakai LY, Rifkin DB (2007). A rapid and sensitive bioassay to measure bone morphogenetic protein activity. BMC Cell Biol 8, 41.
102. Zimmerman LB, De Jesus-Escobar JM, Harland RM (1996). The Spemann organizer signal noggin binds and inactivates bone morphogenetic protein 4. Cell 86, 599-606.