Morphogenesis and cytodifferentiation of the avian retinal pigmented epithelium require downregulation of Group B1 Sox genes

Development

Volumn 136, Issue 15, 2009, Pages 2579-2589

  Ishii, Yasuo ^a   Weinberg, Kerry ^a   Oda Ishii, Izumi ^a   Coughlin, Laura ^a   Mikawa, Takashi ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Chick embryo; Electroporation; Eye; Pigmented epithelium; Retina; Sox genes

Indexed keywords

BETA GALACTOSIDASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SOX1; TRANSCRIPTION FACTOR SOX2; TRANSCRIPTION FACTOR SOX3; TRANSCRIPTION FACTOR SOXB1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL STRUCTURE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DOWN REGULATION; EMBRYO; FOREBRAIN; FOWL; GENE ACTIVITY; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCATION; IMMUNOREACTIVITY; NEURAL CREST; NEUROECTODERM; NONHUMAN; PHENOTYPE; PIGMENT EPITHELIUM; PRIORITY JOURNAL; RETINA DEVELOPMENT; UPREGULATION;

ANIMALS; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CHICKENS; DOWN-REGULATION; FIBROBLAST GROWTH FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MORPHOGENESIS; NEURONS; RETINAL PIGMENT EPITHELIUM; SOXB1 TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION;

AVES;

EID: 69049120328     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.031344     Document Type: Article

References (92)

1. Abu-Elmagd, M., Ishii, Y., Cheung, M., Rex, M., Le Rouëdec, D. and Scotting, P. J. (2001). cSox3 expression and neurogenesis in the epibranchial placodes. Dev. Biol. 237, 258-269.
2. Ambrosetti, D. C., Schöler, H. R., Dailey, L. and Basilico, C. (2000). Modulation of the activity of multiple transcriptional activation domains by the DNA binding domains mediates the synagistic action of Sox2 and Oct-3 on the fibroblast growth factor-4 enhancer. J. Biol. Chem. 275, 23387-23397.
3. Azuma, N., Tadokoro, K., Asaka, A., Yamada, M., Yamaguchi, Y., Handa, H., Matsushima, S., Watanabe, T., Kida, Y., Ogura, T. et al. (2005). Transdifferentiation of the retinal pigment epithelia to the neural retina by transfer of the Pax6 transcriptional factor. Hum. Mol. Genet. 14, 1059-1068.
4. Bovolenta, P., Mallamaci, A., Puelles, L. and Boncinelli, E. (1998). Expression pattern of cSix3, a member of the Six/sine oculis family of transcription factors. Mech. Dev. 70, 201-203.
5. Bowles, J., Schepers, G. and Koopman, P. (2000). Phylogeny of the SOX family of developmental transcription factors based on sequence and structural indicators. Dev. Biol. 227, 239-255.
6. Bruhn, S. L. and Cepko, C. L. (1996). Development of the pattern of photoreceptors in the chick retina. J. Neurosci. 16, 1430-1439.
7. Bumsted, K. M. and Barnstable, C. J. (2000). Dorsal retinal pigment epithelium differentiates as neural retina in the microphthalmia (mi/mi) mouse. Invest. Ophthalmol. Vis. Sci. 41, 903-908.
8. Bylund, M., Andersson, E., Novitch, B. G. and Muhr, J. (2003). Vertebrate neurogenesis is counteracted by Sox1-3 activity. Nat. Neurosci. 6, 1162-1168.
9. Cavallaro, M., Mariani, J., Lancini, C., Latorre, E., Caccia, R., Gullo, F., Valotta, M., DeBiasi, S., Spinardi, L., Ronchi, A. et al. (2008). Impaired generation of mature neurons by neural stem cells from hypomorphic Sox2 mutants. Development 135, 541-557.
10. Chen, C. M. and Cepko, C. L. (2000). Expression of Chx10 and Chx10-1 in the developing chicken retina. Mech. Dev. 90, 293-297.
11. Cheung, M. and Briscoe, J. (2003). Neural crest development is regulated by the transcription factor Sox9. Development 130, 5681-5693.
12. Cheung, M., Chaboissier, M. C., Mynett, A., Hirst, E., Schedl, A. and Briscoe, J. (2005). The transcriptional control of trunk neural crest induction, survival, and delamination. Dev. Cell 8, 179-192.
13. Collignon, J., Sochanathan, S., Hacker, A., Cohen-Tannoudji, M., Norris, D., Rastan, S., Stevanovic, M., Goodfellow, P. N. and Lovell-Badge, R. (1996). A comparison of the properties of Sox-3 with Sry and two related genes, Sox-1 and Sox-2. Development 122, 509-520.
14. Coulombre, J. L. and Coulombre, A. J. (1965). Regeneration of neural retina from the pigmented epithelium in the chick embryo. Dev. Biol. 12, 79-92.
15. Danno, H., Michiue, T., Hitachi, K., Yukita, A., Ishiura, S. and Asashima, M. (2008). Molecular links among the causative genes for ocular malformation: Otx2 and Sox2 coregulate Rax expression. Proc. Natl. Acad. Sci. USA 105, 5408-5413.
16. Das, I., Sparrow, J. R., Lin, M. I., Shih, E., Mikawa, T. and Hempstead, B. L. (2000). Trk C signaling is required for retinal progenitor cell proliferation. J. Neurosci. 20, 2887-2895.
17. Dee, C. T., Hirst, C. S., Shih, Y. H., Tripathi, V. B., Patient, R. K. and Scotting, P. J. (2008). Sox3 regulates both neural fate and differentiation in the zebrafish ectoderm. Dev. Biol. 320, 289-301.
18. Dias da Silva, M. R., Tiffin, N., Mima, T., Mikawa, T. and Hyer, J. (2007). FGF-mediated induction of ciliary body tissue in the chick eye. Dev. Biol. 304, 272-285.
19. Ferri, A. L. M., Cavallaro, M., Braida, D., Di Cristofano, A., Canta, A., Vezzani, A., Ottolenghi, S., Paolo Pandolfi, P., Sala, M., DeBiasi, S. et al. (2004). Sox2 deficiency causes neurodegeneration and impaired neurogenesis in the adult mouse brain. Development 131, 3805-3819.
20. 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.
21. Fukuda, K., Sakamoto, N., Narita, T., Saitoh, K., Kameda, T., Iba, H. and Yasugi, S. (2000). Application of efficient and specific gene transfer systems and organ culture techniques for the elucidation of mechanisms of epithelialmesenchymal interaction in the developing gut. Dev. Growth Differ. 42, 207-211.
22. Furukawa, T., Kozak, C. A. and Cepko, C. L. (1997). rax, a novel paired-type homeobox gene, shows expression in the anterior neural fold and developing retina. Proc. Natl. Acad. Sci. USA 94, 3088-3093.
23. Galy, A., Neron, B., Planque, N., Saule, S. and Eychène, A. (2002). Activated MAPK/ERK kinase (MEK-1) induces transdifferentiation of pigmented epithelium into neural retina. Dev. Biol. 248, 251-264.
24. Graham, V., Khudyakov, J., Ellis, P. and Pevny, L. (2003). SOX2 functions to maintain neural progenitor identity. Neuron 39, 749-765.
25. Guillemot, F. and Cepko, C. L. (1992). Retinal fate and ganglion cell differentiation are potentiated by acidic FGF in an in vitro assay of early retinal development. Development 114, 743-754.
26. Hamburger, V. and Hamilton, J. L. (1951). A series of normal nornal stages in the development of the chick embryo. J. Morphol. 88, 49-92.
27. Hurtado, R. and Mikawa, T. (2006). Enhanced sensitivity and stability in two-color in situ hybridization by means of a novel chromagenic substrate combination. Dev. Dyn. 235, 2811-2816.
28. 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.
29. 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.
30. Inoue, M., Kamachi, Y., Matsunami, H., Imada, K., Uchikawa, M. and Kondoh, H. (2007). PAX6 and SOX2-dependent regulation of the Sox2 enhancer N-3 involved in embryonic visual system development. Genes Cells 12, 1049-1061.
31. Ishii, Y. and Mikawa, T. (2005). Somatic transgenesis in the avian model system. Birth Defects Res. C Embryo Today 75, 19-27.
32. Ishii, Y., Rex, M., Scotting, P. J. and Yasugi, S. (1998). Region-specific expression of chicken Sox2 in the developing gut and lung epithelium: regulation by epithelial-mesenchymal interactions. Dev. Dyn. 213, 464-475.
33. Ishii, Y., Abu-Elmagd, M. and Scotting, P. J. (2001). Sox3 expression defines a common primordium for the epibranchial placodes in chick. Dev. Biol. 236, 344-353.
34. Ishii, Y., Reese, D. E. and Mikawa, T. (2004). Somatic transgenesis using retroviral vectors in the chicken embryo. Dev. Dyn. 229, 630-642.
35. Ishii, Y., Langberg, J. D., Hurtado, R., Lee, S. and Mikawa, T. (2007). Induction of proepicardial marker gene expression by the liver bud. Development 134, 3627-3637.
36. Jean, D., Bernier, G. and Gruss, P. (1999). Six6 (Optx2) is a novel murine Six3-related homeobox gene that demarcates the presumptive pituitary/hypothalamic axis and the ventral optic stalk. Mech. Dev. 84, 31-40.
37. Kamachi, Y., Uchikawa, M., Collignon, J., Lovell-Badge, R. and Kondoh, H. (1998). Involvement of Sox1, 2 and 3 in the early and subsequent molecular events of lens induction. Development 125, 2521-2532.
38. Kamachi, Y., Cheah, K. S. and Kondoh, H. (1999). Mechanism of regulatory target selection by the SOX high-mobility-group domain proteins as revealed by comparison of SOX1/2/3 and SOX9. Mol. Cell. Biol. 19, 107-120.
39. Kamachi, Y., Uchikawa, M. and Kondoh, H. (2000). Pairing SOX off: with partners in the regulation of embryonic development. Trends Genet. 16, 182-187.
40. Kamachi, Y., Uchikawa, M., Tanouchi, A., Sekido, R. and Kondoh, H. (2001). Pax6 and SOX2 form a co-DNA-binding partner complex that regulates initiation of lens development. Genes Dev. 15, 1272-1286.
41. Kan, L., Israsena, N., Zhang, Z, Hu, M., Zhao, L.-R., Jalali, A., Sahni, V. and Kessler, J. A. (2004). Sox1 acts through multiple independent pathways to promote neurogenesis. Dev. Biol. 269, 580-594.
42. Kishi, M., Mizuseki, K., Sasai, N., Yamazaki, H., Shiota, K., Nakanishi, S. and Sasai, Y. (2000). Requirement of Sox2-mediated signaling for differentiation of early Xenopus neuroectoderm. Development 127, 791-800.
43. Kondoh, H., Uchikawa, M. and Kamachi, Y. (2004). Interplay of Pax6 and SOX2 in lens development as a paradigm of genetic switch mechanisms for cell differentiation. Int. J. Dev. Biol. 48, 819-827.
44. Köster, R. W., Kühnlein, R. P. and Wittbrodt, J. (2000). Ectopic Sox3 activity elicits sensory placode formation. Mech. Dev. 95, 175-187.
45. Lee, M. K., Tuttle, J. B., Rebhun, L. I., Cleveland, D. W. and Frankfurter, A. (1990). The expression and posttranslational modification of a neuron-specific beta-tubulin isotype during chick embryogenesis. Cell Motil. Cytoskeleton 17, 118-132.
46. Le Rouëdec, D., Rayner, K., Rex, M., Wigmore, P. M. and Scotting, P. J. (2002). The transcription factor cSox2 and Neuropeptide Y define a novel subgroup of amacrine cells in the retina. J. Anat. 200, 51-56.
47. Li, H. S., Yang, J. M., Jacobson, R. D., Pasco, D. and Sundin, O. (1994). Pax-6 is first expressed in a region of ectoderm anterior to the early neural plate: implications for stepwise determinatin of the lens. Dev. Biol. 162, 181-194.
48. Liu, I. S. C., Chen, J., Ploder, L., Vidgen, D., van der Kooy, D., Kalnins, V. I. and McInnes, R. (1994). Developmental expression of a novel murine homeobox gene (Chx10): Evidence for roles in determination of the neuroretina and inner nuclear layer. Neuron 13, 377-393.
49. Lopashov, G. V. (1963). Developmental Mechanisms of Vertebrate Rudiment. New York: Pergamon Press.
50. López-Ríos, J., Gallardo, M. E., Rodriguez de Córdoba, S. and Bovolenta, P. (1999). Six9 (Optx2), a new member of the six gene family of transcription factors, is expressed at early stages of vertebrate ocular and pituitary development. Mech. Dev. 83, 155-159.
51. Mansukhani, A., Ambrosetti, D., Holmes, G., Cornivelli, L. and Basilico, C. (2005). Sox2 induction by FGF and FGFR2 activating mutations inhibits Wnt signaling and osteoblast differentiation. J. Cell Biol. 168, 1065-1076.
52. Martínez-Morales, J. R., Signore, M., Acampora, D., Simeone, A. and Bovolenta, P. (2001). Otx genes are required for tissue specification in the developing eye. Development 128, 2019-2030.
53. Martínez-Morales, J. R., Dolez, V., Rodrigo, I., Zaccarini, R., Leconte, L., Bovolenta, P. and Saule, S. (2003). Otx2 activates the molecular network underlying retina pigment epithelium differentiation. J. Biol. Chem. 278, 21721-21731.
54. Marusich, M. F., Furneaux, H. M., Henion, P. D. and Weston, J. A. (1994). Hu neuronal proteins are expressed in proliferating neurogenic cells. J. Neurobiol. 25, 143-155.
55. Mathers, P. H., Grinberg, A., Mahon, K. A. and Jamrich, M. (1997). The Rx homeobox gene is essential for vertebrate eye development. Nature 387, 603-607.
56. Matsumata, M., Uchikawa, M., Kamachi, Y. and Kondoh, H. (2005). Multiple N-cadherin enhancers identified by systematic functional screening indicate its Group B1 SOX-dependent regulation in neural and placodal development. Dev. Biol. 286, 601-617.
57. McFarlane, S., Zuber, M. E. and Holt, C. E. (1998). A role for the fibroblast growth factor receptor in cell fate decisions in the developing vertebrate retina. Development 125, 3967-3975.
58. Mikawa, T. (1995). Retroviral targeting of FGF and FGFR in cardiomyocytes and coronary vascular cells during heart development. Ann. NY Acad. Sci. 752, 506-516.
59. Mima, T., Ohuchi, H., Noji, S. and Mikawa, T. (1995a). FGF can induce outgrowth of somatic mesoderm both inside and outside of limb-forming regions. Dev. Biol. 167, 617-620.
60. Mima, T., Ueno, H., Fischman, D. A., Williams, L. T. and Mikawa, T. (1995b). Fibroblast growth factor receptor is required for in vivo cardiac myocyte proliferation at early embryonic stages of heart development. Proc. Natl. Acad. Sci. USA 92, 467-471.
61. Mizuseki, K., Kishi, M., Matsui, M., Nakanishi, S. and Sasai, Y. (1998). Xenopus Zic-related-1 and Sox-2, two factors induced by chordin, have distinct activities in the initiation of neural induction. Development 125, 579-587.
62. Mochii, M., Mazaki, Y., Mizuno, N., Hayashi, H. and Eguchi, G. (1998a). Role of Mitf in differentiation and transdifferentiation of chicken pigmented epithelial cell. Dev. Biol. 193, 47-62.
63. Mochii, M., Ono, T., Matsubara, Y. and Eguchi, G. (1998b). Spontaneous transdifferentiation of quail pigmented epithelial cell is accompanied by a mutation in the Mitf gene. Dev. Biol. 196, 145-159.
64. Moshiri, A., Close, J. and Reh, T. A. (2004). Retinal stem cells and regeneration. Int. J. Dev. Biol. 48, 1003-1014.
65. 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.
66. 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.
67. Nguyen, M. and Arnheiter, H. (2000). Signaling and transcriptional regulation in early mammalian eye development: a link between FGF and MITF. Development 127, 3581-3591.
68. Nitta, K. R., Takahashi, S., Haramoto, Y., Fukuda, M., Onuma, Y. and Asashima, M. (2006). Expression of Sox1 during Xenopus early embryogenesis. Biochem. Biophys. Res. Commun. 351, 287-293.
69. Ohuchi, H., Tomonari, S., Itoh, H., Mikawa, T. and Noji, S. (1999). Identification of chick rax/rx genes with overlapping patterns of expression during early eye and brain development. Mech. Dev. 85, 193-195.
70. Okuda, Y., Yoda, H., Uchikawa, M., Furutani-Seiki, M., Takeda, H., Kondoh, H. and Kamachi, Y. (2006). Comparative genomic and expression analysis of group B1 sox genes in zebrafish indicates their diversification during vertebrate evolution. Dev. Dyn. 235, 811-825.
71. Oliver, G., Mailhos, A., Wehr, R., Copeland, N. G., Jenkins, N. A. and Gruss, P. (1995). Six3, a murine homologue of the sine oculis gene, demarcates the most anterior border of the developing neural plate and is expressed during eye development. Development 121, 4045-4055.
72. Opas, M. and Dziak, E. (1994). bFGF-induced transdifferentiation of RPE to neuronal progenitors is regulated by the mechanical properties of the substratum. Dev. Biol. 161, 440-454.
73. Park, C. M. and Hollenberg, M. J. (1989). Basic fibroblast growth factor induces retinal regeneration in vivo. Dev. Biol. 134, 201-205.
74. Park, C. M. and Hollenberg, M. J. (1991). Induction of retinal regeneration in vivo by growth factors. Dev. Biol. 148, 322-333.
75. Pevny, L. H. and Lovell-Badge, R. (1997). Sox genes find their feet. Curr. Opin. Genet. Dev. 7, 338-344.
76. Pittack, C., Jones, M. and Reh, T. A. (1991). Basic fibroblast growth factor induces retinal pigment epithelium to generate neural retina in vitro. Development 113, 577-588.
77. Pittack, C., Grunwald, G. B. and Reh, T. A. (1997). Fibroblast growth factors are necessary for neural retina but not pigmented epithelium differentiation in chick embryos. Development 124, 805-816.
78. Reh, T. A. and Pittack, C. (1995). Transdifferentiation and retinal regeneration. Semin. Cell Biol. 6, 137-142.
79. Reza, H. M., Takahashi, Y. and Yasuda, K. (2007). Stage-dependent expression of Pax6 in optic vesicle/cup regulates patterning genes through signaling molecules. Differentiation 75, 726-736.
80. Serafini, T., Colamarino, S. A., Leonardo, E. D., Wang, H., Beddington, R., Skarnes, W. C. and Tessier-Lavigne, M. (1996). Netrin-1 is required for commissural axon guidance in the developing vertebrate nervous system. Cell 87, 1001-1014.
81. Tanaka, S., Kamachi, Y., Tanouchi, A., Hamada, H., Jing, N. and Kondoh, H. (2004). Interplay of SOX and POU factors in regulation of the Nestin gene in neural primordial cells. Mol. Cell. Biol. 24, 8834-8846.
82. Taranova, O. V., Magness, S. T., Fagan, B. M., Wu, Y., Surzenko, N., Hutton, S. R. and Pevny, L. H. (2006). SOX2 is a dose-dependent regulator of retinal neural progenitor competence. Genes Dev. 20, 1187-1202.
83. Toy, J. and Sundin, O. H. (1999). Expression of the optx2 homeobox gene during mouse development. Mech. Dev. 83, 183-186.
84. Tsukiji, N., Nishihara, D., Yajima, I., Takeda, K., Shibahara, S. and Yamamoto, H. (2008). Mitf functions as an in ovo regulator for cell differentiation and proliferation during development of the chick RPE. Dev. Biol. 326, 335-346.
85. Uchikawa, M., Kamachi, Y. and Kondoh, H. (1999). Two distinct subgroups of Group B Sox genes for transcriptional activators and repressors: their expression during embryonic organogenesis of the chicken. Mech. Dev. 84, 103-120.
86. Uwanogho, D., Rex, M., Cartwright, E. J., Pearl, G., Healy, C., Scotting, P. J. and Sharpe, P. T. (1995). Embryonic expression of the chicken Sox2, Sox3 and Sox11 genes suggests an interactive role in neuronal development. Mech. Dev. 49, 23-36.
87. Vogel-Höpker, A., Momose, T., Rohrer, H., Yasuda, K., Ishihara, L. and Rapaport, D. H. (2000). Multiple functions of fibroblast growth factor-8 (FGF-8) in chick eye development. Mech. Dev. 94, 25-36.
88. Wood, H. B. and Episkopou, V. (1999). Comparative expression of the mouse Sox1, Sox2 and Sox3 genes from pre-gastrulation to early somite stages. Mech. Dev. 86, 197-201.
89. Yamagata, K., Goto, K., Kuo, C. H., Kondo, H. and Miki, N. (1990). Visinin: a novel calcium binding protein expressed in retinal cone cells. Neuron 2, 469-476.
90. Yoshii, C., Ueda, Y., Okamoto, M. and Araki, M. (2007). Neural retinal regeneration in the anuran amphibian Xenopus laevis post-metamorphosis: Transdifferentiation of retinal pigmented epithelium regenerates the neural retina. Dev. Biol. 303, 45-56.
91. Zhang, L., El-Hodiri, H. M., Ma, H. F., Zhang, X., Servetnick, M., Wensel, T. G. and Jamrich, M. (2003). Targeted expression of the dominant-negative FGFR4a in the eye using Xrx1A regulatory sequences interferes with normal retinal development. Development 130, 4177-4186.
92. Zhao, S., Hung, F. C., Colvin, J. S., White, A., Dai, W., Lovicu, F. J., Ornitz, D. M. and Overbeek, P. A. (2001). Patterning the optic neuroepithelium by FGF signaling and Ras activation. Development 128, 5051-5060.