Canonical Wnt signaling controls proliferation of retinal stem/progenitor cells in postembryonic Xenopus eyes

Stem Cells

Volumn 26, Issue 8, 2008, Pages 2063-2074

  Denayer, Tinneke ^a,b   Locker, Morgane ^c   Borday, Caroline ^c   Deroo, Tom ^a,b   Janssens, Sylvie ^a,b   Hecht, Andreas ^d   Van Roy, Frans ^a,b   Perron, Muriel ^c   Vleminckx, Kris ^a,b,e  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c CNRS   (France)

^d UNIVERSITY OF FREIBURG   (Germany)

^e Technologiepark 927   (Belgium)

Author keywords

Canonical Wnt pathway; Ciliary marginal zone; Proliferation; Retina; Stem cell; Xenopus laevis

Indexed keywords

CYCLIN D1; WNT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL CYCLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL STRAIN HEK293; EMBRYO; GENE ACTIVATION; GENE EXPRESSION; HUMAN; HUMAN CELL; NONHUMAN; RETINA; RETINA CELL; STEM CELL; TRANSCRIPTION REGULATION; TRANSGENIC ANIMAL; XENOPUS;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL PROLIFERATION; EYE; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; HUMANS; MODELS, GENETIC; RETINA; SIGNAL TRANSDUCTION; STEM CELLS; TIME FACTORS; TRANSGENES; WNT PROTEINS; XENOPUS LAEVIS;

VERTEBRATA; XENOPUS LAEVIS;

EID: 55049110120     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1634/stemcells.2007-0900     Document Type: Article

References (67)

1. Ahmad I, Tang L, Pham H. Identification of neural progenitors in the adult mammalian eye. Biochem Biophys Res Commun 2000;270:517-521.
2. Tropepe V, Coles BL, Chiasson BJ et al. Retinal stem cells in the adult mammalian eye. Science 2000;287:2032-2036.
3. Reh TA, Fischer AJ. Stem cells in the vertebrate retina. Brain Behav Evol 2001;58:296-305.
4. Fischer AJ, Reh TA. Potential of Muller glia to become neurogenic retinal progenitor cells. Glia 2003;43:70-76.
5. Coles BL, Angenieux B, Inoue T et al. Facile isolation and the characterization of human retinal stem cells. Proc Natl Acad Sci U S A 2004;101:15772-15777.
6. Amato MA, Arnault E, Perron M. Retinal stem cells in vertebrates: Parallels and divergences. Int J Dev Biol 2004;48:993-1001.
7. Xu H, Sta Iglesia DD, Kielczewski JL et al. Characteristics of progenitor cells derived from adult ciliary body in mouse, rat, and human eyes. Invest Ophthalmol Vis Sci 2007;48:1674-1682.
8. Reh TA. The regulation of neuronal production during retinal neurogenesis. In: Finlay BL and Sengelaub DR, eds. Development of the Vertebrate Retina. New York: Plenum, 1989:43-67.
9. Wetts R, Serbedzija GN, Fraser SE. Cell lineage analysis reveals multipotent precursors in the ciliary margin of the frog retina. Dev Biol 1989;136:254-263.
10. Holt CE, Bertsch TW, Ellis HM et al. Cellular determination in the Xenopus retina is independent of lineage and birth date. Neuron 1988;1:15-26.
11. Dorsky RI, Rapaport DH, Harris WA. Xotch inhibits cell differentiation in the Xenopus retina. Neuron 1995;14:487-496.
12. Perron M, Kanekar S, Vetter ML et al. The genetic sequence of retinal development in the ciliary margin of the Xenopus eye. Dev Biol 1998;199:185-200.
13. Jadhav AP, Cho SH, Cepko CL. Notch activity permits retinal cells to progress through multiple progenitor states and acquire a stem cell property. Proc Natl Acad Sci U S A 2006;103:18998-19003.
14. Perron M, Boy S, Amato MA et al. A novel function for Hedgehog signalling in retinal pigment epithelium differentiation. Development 2003;130:1565-1577.
15. Moshiri A, Reh TA. Persistent progenitors at the retinal margin of ptc+/-mice. J Neurosci 2004;24:229-237.
16. Moshiri A, McGuire CR, Reh TA. Sonic hedgehog regulates proliferation of the retinal ciliary marginal zone in posthatch chicks. Dev Dyn 2005;233:66-75.
17. Wang Y, Dakubo GD, Thurig S et al. Retinal ganglion cell-derived sonic hedgehog locally controls proliferation and the timing of RGC development in the embryonic mouse retina. Development 2005;132:5103-5113.
18. Spence JR, Madhavan M, Ewing JD et al. The hedgehog pathway is a modulator of retina regeneration. Development 2004;131:4607-4621.
19. Shkumatava A, Neumann CJ. Shh directs cell-cycle exit by activating p57Kip2 in the zebrafish retina. EMBO Rep 2005;6:563-569.
20. Masai I, Yamaguchi M, Tonou-Fujimori N et al. The hedgehog-PKA pathway regulates two distinct steps of the differentiation of retinal ganglion cells: The cell-cycle exit of retinoblasts and their neuronal maturation. Development 2005;132:1539-1553.
21. Locker M, Agathocleous M, Amato MA et al. Hedgehog signaling and the retina: Insights into the mechanisms controlling the proliferative properties of neural precursors. Genes Dev 2006;20:3036-3048.
22. Agathocleous M, Locker M, Harris WA et al. A general role of hedgehog in the regulation of proliferation. Cell Cycle 2007;6:156-159.
23. Van Raay TJ, Vetter ML. Wnt/frizzled signaling during vertebrate retinal development. Dev Neurosci 2004;26:352-358.
24. de Iongh RU, Abud HE, Hime GR. WNT/Frizzled signaling in eye development and disease. Front Biosci 2006;11:2442-2464.
25. Kléber M, Sommer L. Wnt signaling and the regulation of stem cell function. Curr Opin Cell Biol 2004;16:681-687.
26. Fuchs E, Tumbar T, Guasch G. Socializing with the neighbors: Stem cells and their niche. Cell 2004;116:769-778.
27. Reya T, Clevers H. Wnt signalling in stem cells and cancer. Nature 2005;434:843-850.
28. Moon RT, Kohn AD, De Ferrari GV et al. WNT and beta-catenin signalling: Diseases and therapies. Nat Rev Genet 2004;5:691-701.
29. Fodde R, Brabletz T. Wnt/beta-catenin signaling in cancer stemness and malignant behavior. Curr Opin Cell Biol 2007;19:150-158.
30. Tetsu O, McCormick F. Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 1999;398:422-426.
31. Shtutman M, Zhurinsky J, Simcha I et al. The cyclin D1 gene is a target of the beta-catenin/LEF-1 pathway. Proc Natl Acad Sci U S A 1999;96:5522-5527.
32. Logan CY, Nusse R. The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 2004;20:781-810.
33. Kimelman D, Xu W. 2006. Beta-catenin destruction complex: Insights and questions from a structural perspective. Oncogene 2006;25:7482-7491.
34. Takeichi M. Cadherin cell adhesion receptors as a morphogenetic regulator. Science 1991;251:1451-1455.
35. Megason SG, McMahon AP. A mitogen gradient of dorsal midline Wnts organizes growth in the CNS. Development 2002;129:2087-2098.
36. Chenn A, Walsh CA. Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science 2002;297:365-369.
37. Viti J, Gulacsi A, Lillien L. Wnt regulation of progenitor maturation in the cortex depends on Shh or fibroblast growth factor 2. J Neurosci 2003;23:5919-5927.
38. Zechner D, Fujita Y, Hulsken J et al. beta-Catenin signals regulate cell growth and the balance between progenitor cell expansion and differentiation in the nervous system. Dev Biol 2003;258:406-418.
39. Israsena N, Hu M, Fu W et al. 2004. The presence of FGF2 signaling determines whether beta-catenin exerts effects on proliferation or neuronal differentiation of neural stem cells. Dev Biol 2004;268:220-231.
40. Adachi K, Mirzadeh Z, Sakaguchi M et al. Beta-catenin signaling promotes proliferation of progenitor cells in the adult mouse subventricular zone. STEM CELLS 2007;25:2827-2836.
41. Hirabayashi Y, Itoh Y, Tabata H et al. The Wnt/beta-catenin pathway directs neuronal differentiation of cortical neural precursor cells. Development 2004;131:2791-2801.
42. Liu H, Mohamed O, Dufort D et al. Characterization of Wnt signaling components and activation of the Wnt canonical pathway in the murine retina. Dev Dyn 2003;227:323-334.
43. Liu H, Thurig S, Mohamed O et al. Mapping canonical Wnt signaling in the developing and adult retina. Invest Ophthalmol Vis Sci 2006;47:5088-5097.
44. Yamaguchi M, Tonou-Fujimori N, Komori A et al. Histone deacetylase 1 regulates retinal neurogenesis in zebrafish by suppressing Wnt and Notch signaling pathways. Development 2005;132:3027-3043.
45. Kubo F, Takeichi M, Nakagawa S. Wnt2b controls retinal cell differentiation at the ciliary marginal zone. Development 2003;130:587-598.
46. Cho SH, Cepko CL. Wnt2b/beta-catenin-mediated canonical Wnt signaling determines the peripheral fates of the chick eye. Development 2006;133:3167-3177.
47. Nakagawa S, Takada S, Takada R et al. Identification of the laminar-inducing factor: Wnt-signal from the anterior rim induces correct laminar formation of the neural retina in vitro. Dev Biol 2003;260:414-425.
48. Kubo F, Takeichi M, Nakagawa S. Wnt2b inhibits differentiation of retinal progenitor cells in the absence of Notch activity by downregulating the expression of proneural genes. Development 2005;132:2759-2770.
49. Liu H, Xu S, Wang Y et al. Ciliary margin transdifferentiation from neural retina is controlled by canonical Wnt signaling. Dev Biol 2007;308:54-67.
50. Das AV, Zhao X, James J et al. Neural stem cells in the adult ciliary epithelium express GFAP and are regulated by Wnt signaling. Biochem Biophys Res Commun 2006;339:708-716.
51. Inoue T, Kagawa T, Fukushima M et al. Activation of canonical Wnt pathway promotes proliferation of retinal stem cells derived from adult mouse ciliary margin. STEM CELLS 2006;24:95-104.
52. Osakada F, Ooto S, Akagi T et al. Wnt signaling promotes regeneration in the retina of adult mammals. J Neurosci 2007;27:4210-4219.
53. Sumanas S, Ekker SC. Xenopus frizzled-5: A frizzled family member expressed exclusively in the neural retina of the developing eye. Mech Dev 2001;103:133-136.
54. Van Raay TJ, Moore KB, Iordanova I et al. Frizzled 5 signaling governs the neural potential of progenitors in the developing Xenopus retina. Neuron 2005;46:23-36.
55. Cavodeassi F, Carreira-Barbosa F, Young RM et al. Early stages of zebrafish eye formation require the coordinated activity of Wnt11, Fz5, and the Wnt/beta-catenin pathway. Neuron 2005;47:43-56.
56. Fu X, Sun H, KleinWHet al. Beta-catenin is essential for lamination but not neurogenesis in mouse retinal development. Dev Biol 2006;299:424-437.
57. Deroo T, Denayer T, Van Roy F et al. Global inhibition of Lef1/Tcf-dependent Wnt signaling at its nuclear end point abrogates development in transgenic Xenopus embryos. J Biol Chem 2004;279:50670-50675.
58. Denayer T, Van Roy F, Vleminckx K. In vivo tracing of canonical Wnt signaling in Xenopus tadpoles by means of an inducible transgenic reporter tool. FEBS Lett 2006;580:393-398.
59. Dullin JP, Locker M, Robach M et al. Ptf1a triggers GABAergic neuronal fates in the retina. BMC Dev Biol 2007;7:110-124.
60. Vleminckx K, Kemler R, Hecht A. The C-terminal transactivation domain of beta-catenin is necessary and sufficient for signaling by the LEF-1/betacatenin complex in Xenopus laevis. Mech Dev 1999;81:65-74.
61. McMahon AP, Moon RT. Ectopic expression of the proto-oncogene int-1 in Xenopus embryos leads to duplication of the embryonic axis. Cell 1989;58:1075-1084.
62. Köster RW, Fraser SE. Tracing transgene expression in living zebrafish embryos. Dev Biol 2001;233:329-346.
63. Clevers H, van de Wetering M. TCF/LEF factor earn their wings. Trends Genet 1997;13:485-489.
64. Bienz M. TCF: Transcriptional activator or repressor? Curr Opin Cell Biol 1998;10:366-372.
65. McGrew LL, Takemaru K, Bates R et al. Direct regulation of the Xenopus engrailed-2 promoter by the Wnt signaling pathway, and a molecular screen for Wnt-responsive genes, confirm a role for Wnt signaling during neural patterning in Xenopus. Mech Dev 1999;87:21-32.
66. Maurus D, Heligon C, Burger-Schwarzler A et al. Noncanonical Wnt-4 signaling and EAF2 are required for eye development in Xenopus laevis. EMBO J 2005;24:1181-1191.
67. Park JS, Valerius MT, McMahon AP. Wnt/beta-catenin signaling regulates nephron induction during mouse kidney development. Development 2007;134:2533-253