RPE specification in the chick is mediated by surface ectoderm-derived BMP and Wnt signalling

Development (Cambridge)

Volumn 140, Issue 24, 2013, Pages 4959-4969

  Steinfeld, Jörg ^a   Steinfeld, Ichie ^a,b   Coronato, Nicola ^a   Hampel, Meggi Lee ^a   Layer, Paul G ^a   Araki, Masasuke ^b   Vogel Höpker, Astrid ^a  

^a DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

^b NARA WOMEN'S UNIVERSITY   (Japan)

Author keywords

Cell fate; Eye; Gsk3 ; Mitf; Optic cup; Optic vesicle patterning; Retinal development; Smad; Vsx2

Indexed keywords

BETA CATENIN; BONE MORPHOGENETIC PROTEIN; GLYCOGEN SYNTHASE KINASE 3BETA; MICROPHTHALMIA ASSOCIATED TRANSCRIPTION FACTOR; SMAD PROTEIN; UNCLASSIFIED DRUG; WNT2 PROTEIN; WNT2B PROTEIN; WNT3A PROTEIN;

ARTICLE; CELL FATE; CHICK EMBRYO; CONTROLLED STUDY; DOWN REGULATION; ECTODERM; EMBRYO; ENZYME INHIBITION; EYE DEVELOPMENT; NONHUMAN; OPTIC DISK CUP; OPTIC VESICLE; PIGMENT EPITHELIUM; PIGMENTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA NEUROEPITHELIAL LAYER; SURFACE ECTODERM; VISUAL NERVOUS SYSTEM; WNT SIGNALING PATHWAY;

CELL FATE; EYE; GSK3Β; MITF; OPTIC CUP; OPTIC VESICLE PATTERNING; RETINAL DEVELOPMENT; SMAD; VSX2;

ANIMALS; BETA CATENIN; BODY PATTERNING; BONE MORPHOGENETIC PROTEINS; CELL DIFFERENTIATION; CHICK EMBRYO; ECTODERM; EYE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLYCOGEN SYNTHASE KINASE 3; MICROPHTHALMIA-ASSOCIATED TRANSCRIPTION FACTOR; RETINAL PIGMENT EPITHELIUM; SMAD PROTEINS; WNT PROTEINS; WNT SIGNALING PATHWAY;

EID: 84888878399     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.096990     Document Type: Article

References (81)

1. Abdul-Ghani, M., Dufort, D., Stiles, R., De Repentigny, Y., Kothary, R. and Megeney, L. A. (2011). Wnt11 promotes cardiomyocyte development by caspase-mediated suppression of canonical Wnt signals. Mol. Cell. Biol. 31, 163-178.
2. Abu-Khalil, A., Fu, L., Grove, E. A., Zecevic, N. and Geschwind, D. H. (2004). Wnt genes define distinct boundaries in the developing human brain: implications for human forebrain patterning. J. Comp. Neurol. 474, 276-288.
3. Adler, R. and Belecky-Adams, T. L. (2002). The role of bone morphogenetic proteins in the differentiation of the ventral optic cup. Development 129, 3161-3171.
4. Adler, R. and Canto-Soler, M. V. (2007). Molecular mechanisms of optic vesicle development: complexities, ambiguities and controversies. Dev. Biol. 305, 1-13.
5. Aoki, H., Hara, A., Nakagawa, S., Motohashi, T., Hirano, M., Takahashi, Y. and Kunisada, T. (2006). Embryonic stem cells that differentiate into RPE cell precursors in vitro develop into RPE cell monolayers in vivo. Exp. Eye Res. 82, 265-274.
6. Bharti, K., Nguyen, M. T., Skuntz, S., Bertuzzi, S. and Arnheiter, H. (2006). The other pigment cell: specification and development of the pigmented epithelium of the vertebrate eye. Pigment Cell Res. 19, 380-394.
7. Bharti, K., Miller, S. S. and Arnheiter, H. (2011). The new paradigm: retinal pigment epithelium cells generated from embryonic or induced pluripotent stem cells. Pigment Cell Melanoma Res. 24, 21-34.
8. Bharti, K., Gasper, M., Ou, J., Brucato, M., Clore-Gronenborn, K., Pickel, J. and Arnheiter, H. (2012). A regulatory loop involving PAX6, MITF, and WNT signaling controls retinal pigment epithelium development. PLoS Genet. 8, e1002757.
9. Broun, M., Gee, L., Reinhardt, B. and Bode, H. R. (2005). Formation of the head organizer in hydra involves the canonical Wnt pathway. Development 132, 2907-2916.
10. Cho, S. H. and Cepko, C. L. (2006). Wnt2b/beta-catenin-mediated canonical Wnt signaling determines the peripheral fates of the chick eye. Development 133, 3167-3177.
11. Clegg, D. O., Buchholz, D., Hikita, S., Rowland, T., Hu, Q. and Johnson, L. V. (2008). RPE cells: development in vivo and derivation from human embryonic stem cells in vitro for treatment of age-related macular degeneration. In Stem Cell Research and Therapeutics (ed. D. O. Clegg and Y. Shi), Chapter 1, pp.1-24. Rotterdam: Springer.
12. Crossley, P. H., Martinez, S., Ohkubo, Y. and Rubenstein, J. L. R. (2001). Coordinate expression of Fgf8, Otx2, Bmp4, and Shh in the rostral prosencephalon during development of the telencephalic and optic vesicles. Neuroscience 108, 183-206.
13. Eiraku, M., Takata, N., Ishibashi, H., Kawada, M., Sakakura, E., Okuda, S., Sekiguchi, K., Adachi, T. and Sasai, Y. (2011). Self-organizing optic-cup morphogenesis in three-dimensional culture. Nature 472, 51-56.
14. Eivers, E., Fuentealba, L. C. and De Robertis, E. M. (2008). Integrating positional information at the level of Smad1/5/8. Curr. Opin. Genet. Dev. 18, 304-310.
15. Fu, X., Sun, H., Klein, W. H. and Mu, X. (2006). Beta-catenin is essential for lamination but not neurogenesis in mouse retinal development. Dev. Biol. 299, 424-437.
16. Fuentealba, L. C., Eivers, E., Ikeda, A., Hurtado, C., Kuroda, H., Pera, E. M. and De Robertis, E. M. (2007). Integrating patterning signals: Wnt/GSK3 regulates the duration of the BMP/Smad1 signal. Cell 131, 980-993.
17. Fuhrmann, S. (2010). Eye morphogenesis and patterning of the optic vesicle. Curr. Top. Dev. Biol. 93, 61-84.
18. Fuhrmann, S., Levine, E. M. and Reh, T. A. (2000). Extraocular mesenchyme patterns the optic vesicle during early eye development in the embryonic chick. Development 127, 4599-4609.
19. Fujimura, N., Taketo, M. M., Mori, M., Korinek, V. and Kozmik, Z. (2009). Spatial and temporal regulation of Wnt/β-catenin signaling is essential for development of the retinal pigment epithelium. Dev. Biol. 334, 31-45.
20. Fujino, T., Asaba, H., Kang, M. J., Ikeda, Y., Sone, H., Takada, S., Kim, D. H., Ioka, R. X., Ono, M., Tomoyori, H. et al. (2003). Low-density lipoprotein receptor-related protein 5 (LRP5) is essential for normal cholesterol metabolism and glucose-induced insulin secretion. Proc. Natl. Acad. Sci. USA 100, 229-234.
21. Furuta, Y., Piston, D. W. and Hogan, B. L. (1997). Bone morphogenetic proteins (BMPs) as regulators of dorsal forebrain development. Development 124, 2203-2212.
22. Garcia-Lopez, R., Vieira, C., Echevarria, D. and Martinez, S. (2004). Fate map of the diencephalon and the zona limitans at the 10-somites stage in chick embryos. Dev. Biol. 268, 514-530.
23. Garcia-Lopez, R., Pombero, A. and Martinez, S. (2009). Fate map of the chick embryo neural tube. Dev. Growth Differ. 51, 145-165.
24. Geetha-Loganathan, P., Nimmagadda, S., Christ, B., Huang, R. and Scaal, M. (2010). Ectodermal Wnt6 is an early negative regulator of limb chondrogenesis in the chicken embryo. BMC Dev. Biol. 10, 32-40.
25. Gessert, S. and Kühl, M. (2010). The multiple phases and faces of wnt signaling during cardiac differentiation and development. Circ. Res. 107, 186-199.
26. Grocott, T., Johnson, S., Bailey, A. P. and Streit, A. (2011). Neural crest cells organize the eye via TGF-β and canonical Wnt signalling. Nat. Commun. 2, 265.
27. Hamburger, V. and Hamilton, H. (1951). A series of normal stages in the development of the chick embryo. J. Morphol. 88, 49-92.
28. Hirashima, M., Kobayashi, T., Uchikawa, M., Kondoh, H. and Araki, M. (2008). Anteroventrally localized activity in the optic vesicle plays a crucial role in the optic development. Dev. Biol. 317, 620-631.
29. Horsford, D. J., Nguyen, M. T., Sellar, G. C., Kothary, R., Arnheiter, H. and McInnes, R. R. (2005). Chx10 repression of Mitf is required for the maintenance of mammalian neuroretinal identity. Development 132, 177-187.
30. Hughes, C. S., Postovit, L. M. and Lajoie, G. A. (2010). Matrigel: a complex protein mixture required for optimal growth of cell culture. Proteomics 10, 1886-1890.
31. Hyer, J., Mima, T. and Mikawa, T. (1998). FGF1 patterns the optic vesicle by directing the placement of the neural retina domain. Development 125, 869-877.
32. Hyer, J., Kuhlman, J., Afif, E. and Mikawa, T. (2003). Optic cup morphogenesis requires pre-lens ectoderm but not lens differentiation. Dev. Biol. 259, 351-363.
33. Ishii, Y., Weinberg, K., Oda-Ishii, I., Coughlin, L. and Mikawa, T. (2009). Morphogenesis and cytodifferentiation of the avian retinal pigmented epithelium require downregulation of Group B1 Sox genes. Development 136, 2579-2589.
34. Kagiyama, Y., Gotouda, N., Sakagami, K., Yasuda, K., Mochii, M. and Araki, M. (2005). Extraocular dorsal signal affects the developmental fate of the optic vesicle and patterns the optic neuroepithelium. Dev. Growth Differ. 47, 523-536.
35. Katoh, M. and Katoh, M. (2007). WNT signaling pathway and stem cell signaling network. Clin. Cancer Res. 13, 4042-4045.
36. Kawano, Y. and Kypta, R. (2003). Secreted antagonists of the Wnt signalling pathway. J. Cell Sci. 116, 2627-2634.
37. Kikuchi, A., Yamamoto, H. and Kishida, S. (2007). Multiplicity of the interactions of Wnt proteins and their receptors. Cell. Signal. 19, 659-671.
38. Klaus, A. and Birchmeier, W. (2008). Wnt signalling and its impact on development and cancer. Nat. Rev. Cancer 8, 387-398.
39. Kobayashi, T., Yasuda, K. and Araki, M. (2010). Coordinated regulation of dorsal bone morphogenetic protein 4 and ventral Sonic hedgehog signaling specifies the dorso-ventral polarity in the optic vesicle and governs ocular morphogenesis through fibroblast growth factor 8 upregulation. Dev. Growth Differ. 52, 351-363.
40. Layer, P. G., Araki, M. and Vogel-Höpker, A. (2010). New concepts for reconstruction of retinal and pigment epithelial tissues. Expert Rev. Ophthalmol. 5, 523-543.
41. Lee, D. H. and Goldberg, A. L. (1998). Proteasome inhibitors: valuable new tools for cell biologists. Trends Cell Biol. 8, 397-403.
42. Liu, W., Lagutin, O., Swindell, E., Jamrich, M. and Oliver, G. (2010). Neuroretina specification in mouse embryos requires Six3-mediated suppression of Wnt8b in the anterior neural plate. J. Clin. Invest. 120, 3568-3577.
43. MacDonald, B. T., Adamska, M. and Meisler, M. H. (2004). Hypomorphic expression of Dkk1 in the doubleridge mouse: dose dependence and compensatory interactions with Lrp6. Development 131, 2543-2552.
44. MacDonald, B. T., Tamai, K. and He, X. (2009). Wnt/β-catenin signaling: components, mechanisms, and diseases. Dev. Cell 17, 9-26.
45. Miller, L. A., Smith, A. N., Taketo, M. M. and Lang, R. A. (2006). Optic cup and facial patterning defects in ocular ectoderm beta-catenin gain-of-function mice. BMC Dev. Biol. 6, 14.
46. Monga, S. P. S., Micsenyi, A., Germinaro, M., Apte, U. and Bell, A. (2006). Beta-Catenin regulation during matrigel-induced rat hepatocyte differentiation. Cell Tissue Res. 323, 71-79.
47. Monteiro, R. M., De Sousa Lopes, S. M., Korchynskyi, O., Ten Dijke, P. and Mummery, C. L. (2004). Spatio-temporal activation of Smad1 and Smad5 in vivo: monitoring transcriptional activity of Smad proteins. J. Cell Sci. 117, 4653-4663.
48. Mukhopadhyay, M., Shtrom, S., Rodriguez-Esteban, C., Chen, L., Tsukui, T., Gomer, L., Dorward, D. W., Glinka, A., Grinberg, A., Huang, S. P. et al. (2001). Dickkopf1 is required for embryonic head induction and limb morphogenesis in the mouse. Dev. Cell 1, 423-434.
49. Müller, F., Rohrer, H. and Vogel-Höpker, A. (2007). Bone morphogenetic proteins specify the retinal pigment epithelium in the chick embryo. Development 134, 3483-3493.
50. Nakano, T., Ando, S., Takata, N., Kawada, M., Muguruma, K., Sekiguchi, K., Saito, K., Yonemura, S., Eiraku, M. and Sasai, Y. (2012). Self-formation of optic cups and storable stratified neural retina from human ESCs. Cell Stem Cell 10, 771-785.
51. Nakayama, A., Nguyen, M. T., Chen, C. C., Opdecamp, K., Hodgkinson, C. A. and Arnheiter, H. (1998). Mutations in microphthalmia, the mouse homolog of the human deafness gene MITF, affect neuroepithelial and neural crest-derived melanocytes differently. Mech. Dev. 70, 155-166.
52. Nguyen, M.-T. and Arnheiter, H. (2000). Signaling and transcriptional regulation in early mammalian eye development: a link between FGF and MITF. Development 127, 3581-3591.
53. Nishihara, D., Yajima, I., Tabata, H., Nakai, M., Tsukiji, N., Katahira, T., Takeda, K., Shibahara, S., Nakamura, H. and Yamamoto, H. (2012). Otx2 is involved in the regional specification of the developing retinal pigment epithelium by preventing the expression of sox2 and fgf8, factors that induce neural retina differentiation. PLoS ONE 7, e48879.
54. Ohkubo, Y., Chiang, C. and Rubenstein, J. L. (2002). Coordinate regulation and synergistic actions of BMP4, SHH and FGF8 in the rostral prosencephalon regulate morphogenesis of the telencephalic and optic vesicles. Neuroscience 111, 1-17.
55. Ohta, K., Ito, A., Kuriyama, S., Lupo, G., Kosaka, M., Ohnuma, S., Nakagawa, S. and Tanaka, H. (2011). Tsukushi functions as a Wnt signaling inhibitor by competing with Wnt2b for binding to transmembrane protein Frizzled4. Proc. Natl. Acad. Sci. USA 108, 14962-14967.
56. Osakada, F., Ikeda, H., Sasai, Y. and Takahashi, M. (2009). Stepwise differentiation of pluripotent stem cells into retinal cells. Nat. Protoc. 4, 811-824.
57. Ou, J., Bharti, K., Nodari, A., Bertuzzi, S. and Arnheiter, H. (2013). Vax1/2 genes counteract Mitf-induced respecification of the retinal pigment epithelium. PLoS ONE 8, e59247.
58. Patthey, C., Edlund, T. and Gunhaga, L. (2009). Wnt-regulated temporal control of BMP exposure directs the choice between neural plate border and epidermal fate. Development 136, 73-83.
59. Pera, E. M., Ikeda, A., Eivers, E. and De Robertis, E. M. (2003). Integration of IGF, FGF, and anti-BMP signals via Smad1 phosphorylation in neural induction. Genes Dev. 17, 3023-3028.
60. Pombero, A. and Martinez, S. (2009). Telencephalic morphogenesis during the process of neurulation: an experimental study using quail-chick chimeras. J. Comp. Neurol. 512, 784-797.
61. Qiu, W., Chen, L. and Kassem, M. (2011). Activation of non-canonical Wnt/JNK pathway by Wnt3a is associated with differentiation fate determination of human bone marrow stromal (mesenchymal) stem cells. Biochem. Biophys. Res. Commun. 413, 98-104.
62. Qu, F., Wang, J., Xu, N., Liu, C., Li, S., Wang, N., Qi, W., Li, H., Li, C., Geng, Z. et al. (2013). WNT3A modulates chondrogenesis via canonical and non-canonical Wnt pathways in MSCs. Front. Biosci. 18, 493-503.
63. Quinlan, R., Graf, M., Mason, I., Lumsden, A. and Kiecker, C. (2009). Complex and dynamic patterns of Wnt pathway gene expression in the developing chick forebrain. Neural Dev. 4, 35.
64. Ramel, M. C., Buckles, G. R., Baker, K. D. and Lekven, A. C. (2005). WNT8 and BMP2B co-regulate non-axial mesoderm patterning during zebrafish gastrulation. Dev. Biol. 287, 237-248.
65. Rossi, E., Siwiec, F. and Yan, C. Y. I. (2007). Pattern of Wnt ligand expression during chick eye development. Braz. J. Med. Biol. Res. 40, 1333-1338.
66. Rowan, S., Chen, C. M., Young, T. L., Fisher, D. E. and Cepko, C. L. (2004). Transdifferentiation of the retina into pigmented cells in ocular retardation mice defines a new function of the homeodomain gene Chx10. Development 131, 5139-5152.
67. Sasai, Y. (2013). Cytosystems dynamics in self-organization of tissue architecture. Nature 493, 318-326.
68. Sasai, Y., Eiraku, M. and Suga, H. (2012). In vitro organogenesis in three dimensions: self-organising stem cells. Development 139, 4111-4121.
69. Smith, A. N., Miller, L. A., Song, N., Taketo, M. M. and Lang, R. A. (2005). The duality of beta-catenin function: a requirement in lens morphogenesis and signaling suppression of lens fate in periocular ectoderm. Dev. Biol. 285, 477-489.
70. Szeto, D. P. and Kimelman, D. (2004). Combinatorial gene regulation by Bmp and Wnt in zebrafish posterior mesoderm formation. Development 131, 3751-3760.
71. Teraoka, M. E., Paschaki, M., Muta, Y. and Ladher, R. K. (2009). Rostral paraxial mesoderm regulates refinement of the eye field through the bone morphogenetic protein (BMP) pathway. Dev. Biol. 330, 389-398.
72. Tsukiyama, T. and Yamaguchi, T. P. (2012). Mice lacking Wnt2b are viable and display a postnatal olfactory bulb phenotype. Neurosci. Lett. 512, 48-52.
73. van Amerongen, R. and Berns, A. (2006). Knockout mouse models to study Wnt signal transduction. Trends Genet. 22, 678-689.
74. Van Raay, T. J. and Vetter, M. L. (2004). Wnt/frizzled signaling during vertebrate retinal development. Dev. Neurosci. 26, 352-358.
75. Veien, E. S., Rosenthal, J. S., Kruse-Bend, R. C., Chien, C.-B. and Dorsky, R. I. (2008). Canonical Wnt signaling is required for the maintenance of dorsal retinal identity. Development 135, 4101-4111.
76. Westenskow, P., Piccolo, S. and Fuhrmann, S. (2009). β-catenin controls differentiation of the retinal pigment epithelium in the mouse optic cup by regulating Mitf and Otx2 expression. Development 136, 2505-2510.
77. Westenskow, P. D., McKean, J. B., Kubo, F., Nakagawa, S. and Fuhrmann, S. (2010). Ectopic Mitf in the embryonic chick retina by co-transfection of β-catenin and Otx2. Invest. Ophthalmol. Vis. Sci. 51, 5328-5335.
78. Wilson, S. I., Rydström, A., Trimborn, T., Willert, K., Nusse, R., Jessell, T. M. and Edlund, T. (2001). The status of Wnt signalling regulates neural and epidermal fates in the chick embryo. Nature 411, 325-330.
79. Zakin, L. D., Mazan, S., Maury, M., Martin, N., Guénet, J.-L. and Brûlet, P. (1998). Structure and expression of Wnt13, a novel mouse Wnt2 related gene. Mech. Dev. 73, 107-116.
80. Zechner, D., Müller, T., Wende, H., Walther, I., Taketo, M. M., Crenshaw, E. B., 3rd, Treier, M., Birchmeier, W. and Birchmeier, C. (2007). Bmp and Wnt/beta-catenin signals control expression of the transcription factor Olig3 and the specification of spinal cord neurons. Dev. Biol. 303, 181-190.
81. Zhou, C. J., Molotkov, A., Song, L., Li, Y., Pleasure, D. E., Pleasure, S. J. and Wang, Y. Z. (2008). Ocular coloboma and dorsoventral neuroretinal patterning defects in Lrp6 mutant eyes. Dev. Dyn. 237, 3681-3689.