Specification of embryonic stem cell-derived tissues into eye fields by Wnt signaling using rostral diencephalic tissue-inducing culture

Mechanisms of Development

Volumn 141, Issue , 2016, Pages 90-99

  Sakakura, Eriko ^a   Eiraku, Mototsugu ^a   Takata, Nozomu ^a,b  

^a RIKEN Center for Biosystems Dynamics Research   (Japan)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Embryonic stem cells; Eye field; Optic vesicle; Rax; Rostral diencephalon; Wnt signaling

Indexed keywords

NERVE CELL ADHESION MOLECULE; TRANSCRIPTION FACTOR SOX1; AXIN; AXIN2 PROTEIN, MOUSE; EYE PROTEIN; HOMEODOMAIN PROTEIN; RAX PROTEIN, MOUSE; TRANSCRIPTION FACTOR; VSX2 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AXIN2 GENE; CELL AGGREGATION; CELL DIFFERENTIATION; CONTROLLED STUDY; DIENCEPHALON; EMBRYO; EMBRYONIC STEM CELL; EYE DEVELOPMENT; GENE EXPRESSION; HUMAN; HUMAN CELL; HYPOTHALAMUS; MARKER GENE; MOUSE; NONHUMAN; PRIMORDIUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; ROSTRAL DIENCEPHALON; WNT SIGNALING PATHWAY; ANIMAL; CELL LINEAGE; DRUG EFFECTS; EMBRYO DEVELOPMENT; EMBRYOLOGY; EYE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; RETINA; THALAMUS INTRALAMINAR NUCLEUS; WNT SIGNALING;

ANIMALS; AXIN PROTEIN; CELL DIFFERENTIATION; CELL LINEAGE; DIENCEPHALON; EMBRYONIC DEVELOPMENT; EMBRYONIC STEM CELLS; EYE; EYE PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; INTRALAMINAR THALAMIC NUCLEI; MICE; RETINA; TRANSCRIPTION FACTORS; WNT SIGNALING PATHWAY;

EID: 84971667869     PISSN: 09254773     EISSN: 18726356     Source Type: Journal    
DOI: 10.1016/j.mod.2016.05.001     Document Type: Article

References (56)

1. Assawachananont, J., Mandai, M., Okamoto, S., Yamada, C., Eiraku, M., Yonemura, S., Sasai, Y., Takahashi, M., Transplantation of embryonic and induced pluripotent stem cell-derived 3D retinal sheets into retinal degenerative mice. Stem Cell Reports. 2 (2014), 662–674.
2. Aubert, J., Stavridis, M.P., Tweedie, S., O'Reilly, M., Vierlinger, K., Li, M., Ghazal, P., Pratt, T., Mason, J.O., Roy, D., Smith, A., Screening for mammalian neural genes via fluorescence-activated cell sorter purification of neural precursors from Sox1-gfp knock-in mice. Proc. Natl. Acad. Sci. U. S. A. 100 (2003), 11836–11841 Suppl 1.
3. Bach, A., Lallemand, Y., Nicola, M.A., Ramos, C., Mathis, L., Maufras, M., Robert, B., Msx1 is required for dorsal diencephalon patterning. Development 130 (2003), 4025–4036.
4. Bailey, T.J., El-Hodiri, H., Zhang, L., Shah, R., Mathers, P.H., Jamrich, M., Regulation of vertebrate eye development by Rx genes. Int J Dev sBiol. 48 (2004), 761–770.
5. Bouhon, I.A., Kato, H., Chandran, S., Allen, N.D., Neural differentiation of mouse embryonic stem cells in chemically defined medium. Brain Res. Bull. 68 (2005), 62–75.
6. Burns, C.J., Zhang, J., Brown, E.C., Van Bibber, A.M., Van Es, J., Clevers, H., Ishikawa, T.O., Taketo, M.M., Vetter, M.L., Fuhrmann, S., Investigation of Frizzled-5 during embryonic neural development in mouse. Dev. Dyn. 237 (2008), 1614–1626.
7. Cai, Z.G., Feng, G.S., Zhang, X., Temporal requirement of the protein tyrosine phosphatase Shp2 in establishing the neuronal fate in early retinal development. J. Neurosci. 30 (2010), 4110–4119.
8. Casarosa, S., Andreazzoli, M., Simeone, A., Barsacchi, G., Xrx1, a novel Xenopus homeobox gene expressed during eye and pineal gland development. Mech. Dev. 61 (1997), 187–198.
9. Cavodeassi, F., Carreira-Barbosa, F., Young, R.M., Concha, M.L., Allende, M.L., Houart, C., Tada, M., Wilson, S.W., Early stages of zebrafish eye formation require the coordinated activity of Wnt11, Fz5, and the Wnt/beta-catenin pathway. Neuron 47 (2005), 43–56.
10. Cepko, C., Intrinsically different retinal progenitor cells produce specific types of progeny. Nat. Rev. Neurosci. 15 (2014), 615–627.
11. Chen, B., Dodge, M.E., Tang, W., Lu, J., Ma, Z., Fan, C.W., Wei, S., Hao, W., Kilgore, J., Williams, N.S., Roth, M.G., Amatruda, J.F., Chen, C., Lum, L., Small molecule-mediated disruption of Wnt-dependent signaling in tissue regeneration and cancer. Nat. Chem. Biol. 5 (2009), 100–107.
12. Cho, S.H., Cepko, C.L., Wnt2b/beta-catenin-mediated canonical Wnt signaling determines the peripheral fates of the chick eye. Development 133 (2006), 3167–3177.
13. Corson, L.B., Yamanaka, Y., Lai, K.M., Rossant, J., Spatial and temporal patterns of ERK signaling during mouse embryogenesis. Development 130 (2003), 4527–4537.
14. Dodge, M.E., Moon, J., Tuladhar, R., Lu, J., Jacob, L.S., Zhang, L.S., Shi, H., Wang, X., Moro, E., Mongera, A., Argenton, F., Karner, C.M., Carroll, T.J., Chen, C., Amatruda, J.F., Lum, L., Diverse chemical scaffolds support direct inhibition of the membrane-bound O-acyltransferase porcupine. J. Biol. Chem. 287 (2012), 23246–23254.
15. Eiraku, M., Adachi, T., Sasai, Y., Relaxation-expansion model for self-driven retinal morphogenesis: a hypothesis from the perspective of biosystems dynamics at the multi-cellular level. BioEssays 34 (2012), 17–25.
16. Eiraku, M., Sasai, Y., Mouse embryonic stem cell culture for generation of three-dimensional retinal and cortical tissues. Nat. Protoc. 7 (2012), 69–79.
17. Eiraku, M., Takata, N., Ishibashi, H., Kawada, M., Sakakura, E., Okuda, S., Sekiguchi, K., Adachi, T., Sasai, Y., Self-organizing optic-cup morphogenesis in three-dimensional culture. Nature 472 (2011), 51–U73.
18. Fuhrmann, S., Eye morphogenesis and patterning of the optic vesicle. Curr. Top. Dev. Biol. 93 (2010), 61–84.
19. Fuhrmann, S., Riesenberg, A.N., Mathiesen, A.M., Brown, E.C., Vetter, M.L., Brown, N.L., Characterization of a transient TCF/LEF-responsive progenitor population in the embryonic mouse retina. Invest. Ophthalmol. Vis. Sci. 50 (2009), 432–440.
20. Fujimura, N., Taketo, M.M., Mori, M., Korinek, V., Kozmik, Z., Spatial and temporal regulation of Wnt/beta-catenin signaling is essential for development of the retinal pigment epithelium. Dev. Biol. 334 (2009), 31–45.
21. Furukawa, T., Kozak, C.A., Cepko, C.L., Rax, a novel paired-type homeobox gene, shows expression in the anterior neural fold and developing retina. Proc. Natl. Acad. Sci. U. S. A. 94 (1997), 3088–3093.
22. Gonzalez-Cordero, A., West, E.L., Pearson, R.A., Duran, Y., Carvalho, L.S., Chu, C.J., Naeem, A., Blackford, S.J.I., Georgiadis, A., Lakowski, J., Hubank, M., Smith, A.J., Bainbridge, J.W.B., Sowden, J.C., Ali, R.R., Photoreceptor precursors derived from three-dimensional embryonic stem cell cultures integrate and mature within adult degenerate retina. Nat. Biotechnol., 31, 2013, 741.
23. Graw, J., Eye development. Curr. Top. Dev. Biol. 90 (2010), 343–386.
24. Hyer, J., Mima, T., Mikawa, T., FGF1 patterns the optic vesicle by directing the placement of the neural retina domain. Development 125 (1998), 869–877.
25. Jho, E.H., Zhang, T., Domon, C., Joo, C.K., Freund, J.N., Costantini, F., Wnt/beta-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol. Cell. Biol. 22 (2002), 1172–1183.
26. Lagutin, O.V., Zhu, C.C., Kobayashi, D., Topczewski, J., Shimamura, K., Puelles, L., Russell, H.R., McKinnon, P.J., Solnica-Krezel, L., Oliver, G., Six3 repression of Wnt signaling in the anterior neuroectoderm is essential for vertebrate forebrain development. Genes Dev. 17 (2003), 368–379.
27. Lavado, A., Lagutin, O.V., Oliver, G., Six3 inactivation causes progressive caudalization and aberrant patterning of the mammalian diencephalon. Development 135 (2008), 441–450.
28. Li, H.S., Tierney, C., Wen, L., Wu, J.Y., Rao, Y., A single morphogenetic field gives rise to two retina primordia under the influence of the prechordal plate. Development 124 (1997), 603–615.
29. Liu, W., Focus on molecules: Wnt8b: a suppressor of early eye and retinal progenitor formation. Exp. Eye Res. 101 (2012), 113–114.
30. Liu, W., Lagutin, O., Swindell, E., Jamrich, M., Oliver, G., Neuroretina specification in mouse embryos requires Six3-mediated suppression of Wnt8b in the anterior neural plate. J. Clin. Invest. 120 (2010), 3568–3577.
31. Loosli, F., Staub, W., Finger-Baier, K.C., Ober, E.A., Verkade, H., Wittbrodt, J., Baier, H., Loss of eyes in zebrafish caused by mutation of chokh/rx3. EMBO Rep. 4 (2003), 894–899.
32. Loosli, F., Winkler, S., Burgtorf, C., Wurmbach, E., Ansorge, W., Henrich, T., Grabher, C., Arendt, D., Carl, M., Krone, A., Grzebisz, E., Wittbrodt, J., Medaka eyeless is the key factor linking retinal determination and eye growth. Development 128 (2001), 4035–4044.
33. Mathers, P.H., Grinberg, A., Mahon, K.A., Jamrich, M., The Rx homeobox gene is essential for vertebrate eye development. Nature 387 (1997), 603–607.
34. Muguruma, K., Nishiyama, A., Ono, Y., Miyawaki, H., Mizuhara, E., Hori, S., Kakizuka, A., Obata, K., Yanagawa, Y., Hirano, T., Sasai, Y., Ontogeny-recapitulating generation and tissue integration of ES cell-derived Purkinje cells. Nat. Neurosci. 13 (2010), 1171–1180.
35. Nakano, T., Ando, S., Takata, N., Kawada, M., Muguruma, K., Sekiguchi, K., Saito, K., Yonemura, S., Eiraku, M., Sasai, Y., Self-formation of optic cups and storable stratified neural retina from human ESCs. Cell Stem Cell 10 (2012), 771–785.
36. Nasu, M., Takata, N., Danjo, T., Sakaguchi, H., Kadoshima, T., Futaki, S., Sekiguchi, K., Eiraku, M., Sasai, Y., Robust formation and maintenance of continuous stratified cortical neuroepithelium by laminin-containing matrix in mouse ES cell culture. PLoS One, 7, 2012, e53024.
37. Nguyen, M.T.T., Arnheiter, H., Signaling and transcriptional regulation in early mammalian eye development: a link between FGF and MITF. Development 127 (2000), 3581–3591.
38. Parr, B.A., Shea, M.J., Vassileva, G., Mcmahon, A.P., Mouse Wnt genes exhibit discrete domains of expression in the early embryonic Cns and limb buds. Development 119 (1993), 247–261.
39. Pelletier, J.C., Lundquist, J.T., Gilbert, A.M., Alon, N., Bex, F.J., Bhat, B.M., Bursavich, M.G., Coleburn, V.E., Felix, L.A., Green, D.M., Green, P., Hauze, D.B., Kharode, Y.P., Lam, H.S., Lockhead, S.R., Magolda, R.L., Matteo, J.J., Mehlmann, J.F., Milligan, C., Murrills, R.J., Pirrello, J., Selim, S., Sharp, M.C., Unwalla, R.J., Vera, M.D., Wrobel, J.E., Yaworsky, P., Bodine, P.V.N., (1-(4-(Naphthalen-2-yl)pyrimidin-2-yl)piperidin-4-yl)methanamine: a Wingless beta-Catenin Agonist That Increases Bone Formation Rate. J. Med. Chem. 52 (2009), 6962–6965.
40. Roelink, H., Nusse, R., Expression of two members of the Wnt family during mouse development–restricted temporal and spatial patterns in the developing neural tube. Genes Dev. 5 (1991), 381–388.
41. Rowan, S., Cepko, C.L., Genetic analysis of the homeodomain transcription factor Chx10 in the retina using a novel multifunctional BAC transgenic mouse reporter. Dev. Biol. 271 (2004), 388–402.
42. Shamir, E.R., Ewald, A.J., Three-dimensional organotypic culture: experimental models of mammalian biology and disease. Nat. Rev. Mol. Cell Biol. 15 (2014), 647–664.
43. Suga, H., Kadoshima, T., Minaguchi, M., Ohgushi, M., Soen, M., Nakano, T., Takata, N., Wataya, T., Muguruma, K., Miyoshi, H., Yonemura, S., Oiso, Y., Sasai, Y., Self-formation of functional adenohypophysis in three-dimensional culture. Nature 480 (2011), 57–U215.
44. Takada, R., Satomi, Y., Kurata, T., Ueno, N., Norioka, S., Kondoh, H., Takao, T., Takada, S., Monounsaturated fatty acid modification of Wnt protein: its role in Wnt secretion. Dev. Cell 11 (2006), 791–801.
45. Takata, N., Sakakura, E., Sasai, Y., Activation of Wnt/ss-Catenin Signaling in ESC Promotes Rostral Forebrain Differentiation in Vitro. 2015 (In Vitro Cell Dev Biol Anim).
46. Theil, T., Aydin, S., Koch, S., Grotewold, L., Ruther, U., Wnt and Bmp signalling cooperatively regulate graded Emx2 expression in the dorsal telencephalon. Development 129 (2002), 3045–3054.
47. Tickle, C., Patterning in Vertebrate Development. 2002, Oxford University Press, Oxford; New York.
48. Voronina, V.A., Kozhemyakina, E.A., O'Kernick, C.M., Kahn, N.D., Wenger, S.L., Linberg, J.V., Schneider, A.S., Mathers, P.H., Mutations in the human RAX homeobox gene in a patient with anophthalmia and sclerocornea. Hum. Mol. Genet. 13 (2004), 315–322.
49. Wataya, T., Ando, S., Muguruma, K., Ikeda, H., Watanabe, K., Eiraku, M., Kawada, M., Takahashi, J., Hashimoto, N., Sasai, Y., Minimization of exogenous signals in ES cell culture induces rostral hypothalamic differentiation. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 11796–11801.
50. Westenskow, P., Piccolo, S., Fuhrmann, S., Beta-catenin controls differentiation of the retinal pigment epithelium in the mouse optic cup by regulating Mitf and Otx2 expression. Development 136 (2009), 2505–2510.
51. Wiles, M.V., Johansson, B.M., Embryonic stem cell development in a chemically defined medium. Exp. Cell Res. 247 (1999), 241–248.
52. Wilson, S.W., Houart, C., Early steps in the development of the forebrain. Dev. Cell 6 (2004), 167–181.
53. Yang, X.J., Roles of cell-extrinsic growth factors in vertebrate eye pattern formation and retinogenesis. Semin. Cell Dev. Biol. 15 (2004), 91–103.
54. Yao, Y., Li, W., Wu, J.W., Germann, U.A., Su, M.S.S., Kuida, K., Boucher, D.M., Extracellular signal-regulated kinase 2 is necessary for mesoderm differentiation. Proc. Natl. Acad. Sci. U. S. A. 100 (2003), 12759–12764.
55. Zaghloul, N.A., Yan, B., Moody, S.A., Step-wise specification of retinal stem cells during normal embryogenesis. Biol. Cell. 97 (2005), 321–337.
56. Takata, N., Eiraku, M., Sakakura, E., Dataset describing Rax positive optic-vesicle generation from mouse embryonic stem cells in vitro., 2016 Data in Brief (submitted).