Roles for Dicer1 in the patterning and differentiation of the optic cup neuroepithelium

Development

Volumn 138, Issue 1, 2011, Pages 127-138

  Davis, Noa ^a   Mor, Eyal ^a   Ashery Padan, Ruth ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

Ciliary body; Dicer1; Iris; MicroRNAs; Mouse; Optic cup; Retinogenesis

Indexed keywords

DICER; DICER1 ENZYME; MICRORNA; NOTCH RECEPTOR; SONIC HEDGEHOG PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL POPULATION; CELL PROLIFERATION; CELL STRUCTURE; CILIARY BODY; CONTROLLED STUDY; ENZYME ACTIVATION; FEMALE; MORPHOGENESIS; MOUSE; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NEUROEPITHELIUM; NONHUMAN; OPTIC DISK CUP; PHENOTYPE; PHOTORECEPTOR CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; RETINA AMACRINE CELL; RNA SYNTHESIS;

AMACRINE CELLS; ANIMALS; CELL DIFFERENTIATION; CILIARY BODY; DEAD-BOX RNA HELICASES; ENDORIBONUCLEASES; EYE; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IRIS; MICE; MICE, TRANSGENIC; MICRORNAS; PHOTORECEPTOR CELLS, VERTEBRATE; PREGNANCY; RETINA; RETINAL GANGLION CELLS;

ERINACEIDAE;

EID: 78650754285     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.053637     Document Type: Article

References (89)

1. Ahmad, I., Tang, L. and Pham, H. (2000). Identification of neural progenitors in the adult mammalian eye. Biochem. Biophys. Res. Commun. 270, 517-521.
2. Baek, D., Villen, J., Shin, C., Camargo, F. D., Gygi, S. P. and Bartel, D. P. (2008). The impact of microRNAs on protein output. Nature 455, 64-71.
3. Bao, Z. Z. and Cepko, C. L. (1997). The expression and function of Notch pathway genes in the developing rat eye. J. Neurosci. 17, 1425-1434.
4. Bernstein, E., Kim, S. Y., Carmell, M. A., Murchison, E. P., Alcorn, H., Li, M. Z., Mills, A. A., Elledge, S. J., Anderson, K. V. and Hannon, G. J. (2003). Dicer is essential for mouse development. Nat. Genet. 35, 215-217.
5. 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.
6. Calera, M. R., Topley, H. L., Liao, Y., Duling, B. R., Paul, D. L. and Goodenough, D. A. (2006). Connexin43 is required for production of the aqueous humor in the murine eye. J. Cell Sci. 119, 4510-4519.
7. Coffey, K. L., Krushinsky, A., Green, C. R. and Donaldson, P. J. (2002). Molecular profiling and cellular localization of connexin isoforms in the rat ciliary epithelium. Exp. Eye Res. 75, 9-21.
8. Cvekl, A. and Tamm, E. R. (2004). Anterior eye development and ocular mesenchyme: new insights from mouse models and human diseases. BioEssays 26, 374-386.
9. Dakubo, G. D., Beug, S. T., Mazerolle, C. J., Thurig, S., Wang, Y. and Wallace, V. A. (2008). Control of glial precursor cell development in the mouse optic nerve by sonic hedgehog from retinal ganglion cells. Brain Res. 1228, 27-42.
10. Damiani, D., Alexander, J. J., O'rourke, J. R., McManus, M., Jadhav, A. P., Cepko, C. L., Hauswirth, W. W., Harfe, B. D. and Strettoi, E. (2008). Dicer inactivation leads to progressive functional and structural degeneration of the mouse retina. J. Neurosci. 28, 4878-4887.
11. Davis-Silberman, N. and Ashery-Padan, R. (2008). Iris development in vertebrates; genetic and molecular considerations. Brain Res. 1192, 17-28.
12. Davis-Silberman, N., Kalich, T., Oron-Karni, V., Marquardt, T., Kroeber, M., Tamm, E. R. and Ashery-Padan, R. (2005). Genetic dissection of Pax6 dosage requirements in the developing mouse eye. Hum. Mol. Genet. 14, 2265-2276.
13. Davis, N., Yoffe, C., Raviv, S., Antes, R., Berger, J., Holzmann, S., Stoykova, A., Overbeek, P. A., Tamm, E. R. and Ashery-Padan, R. (2009). Pax6 dosage requirements in iris and ciliary body differentiation. Dev. Biol. 333, 132-142.
14. Davis, T. H., Cuellar, T. L., Koch, S. M., Barker, A. J., Harfe, B. D., McManus, M. T. and Ullian, E. M. (2008). Conditional loss of Dicer disrupts cellular andtissue morphogenesis in the cortex and hippocampus. J. Neurosci. 28, 4322-4330.
15. Decembrini, S., Andreazzoli, M., Barsacchi, G. and Cremisi, F. (2008). Dicer inactivation causes heterochronic retinogenesis in Xenopus laevis. Int. J. Dev. Biol. 52, 1099-1103.
16. Dyer, M. A. and Cepko, C. L. (2000). p57(Kip2) regulates progenitor cell proliferation and amacrine interneuron development in the mouse retina. Development 127, 3593-3605.
17. Esteve, P. and Bovolenta, P. (2006). Secreted inducers in vertebrate eye development: more functions for old morphogens. Curr. Opin. Neurobiol. 16, 13-19.
18. Feng, L., Xie, X., Joshi, P. S., Yang, Z., Shibasaki, K., Chow, R. L. and Gan, L. (2006). Requirement for Bhlhb5 in the specification of amacrine and cone bipolar subtypes in mouse retina. Development 133, 4815-4825.
19. Fischer, A. J. and Reh, T. A. (2000). Identification of a proliferating marginal zone of retinal progenitors in postnatal chickens. Dev. Biol. 220, 197-210.
20. Fischer, A. J. and Reh, T. A. (2001). Transdifferentiation of pigmented epithelial cells: a source of retinal stem cells? Dev. Neurosci. 23, 268-276.
21. Friedman, L. M., Dror, A. A., Mor, E., Tenne, T., Toren, G., Satoh, T., Biesemeier, D. J., Shomron, N., Fekete, D. M., Hornstein, E. et al. (2009a). MicroRNAs are essential for development and function of inner ear hair cells in vertebrates. Proc. Natl. Acad. Sci. USA 106, 7915-7920.
22. Friedman, R. C., Farh, K. K., Burge, C. B. and Bartel, D. P. (2009b). Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 19, 92-105.
23. Fujitani, Y., Fujitani, S., Luo, H., Qiu, F., Burlison, J., Long, Q., Kawaguchi, Y., Edlund, H., MacDonald, R. J., Furukawa, T. et al. (2006). Ptf1a determines horizontal and amacrine cell fates during mouse retinal development. Development 133, 4439-4450.
24. Furimsky, M. and Wallace, V. A. (2006). Complementary Gli activity mediates early patterning of the mouse visual system. Dev. Dyn. 235, 594-605.
25. Furukawa, T., Morrow, E. M. and Cepko, C. L. (1997). Crx, a novel otx-like homeobox gene, shows photoreceptor-specific expression and regulates photoreceptor differentiation. Cell 91, 531-541.
26. Georgi, S. A. and Reh, T. A. (2010). Dicer is required for the transition from early to late progenitor state in the developing mouse retina. J. Neurosci. 30, 4048-4061.
27. Giraldez, A. J., Mishima, Y., Rihel, J., Grocock, R. J., Van Dongen, S., Inoue, K., Enright, A. J. and Schier, A. F. (2006). Zebrafish MiR-430 promotes deadenylation and clearance of maternal mRNAs. Science 312, 75-79.
28. Gould, D. B., Smith, R. S. and John, S. W. (2004). Anterior segment development relevant to glaucoma. Int. J. Dev. Biol. 48, 1015-1029.
29. Graw, J. (1996). Genetic aspects of embryonic eye development in vertebrates. Dev. Genet. 18, 181-197.
30. Grishok, A., Pasquinelli, A. E., Conte, D., Li, N., Parrish, S., Ha, I., Baillie, D. L., Fire, A., Ruvkun, G. and Mello, C. C. (2001). Genes and mechanisms related to RNA interference regulate expression of the small temporal RNAs that control C. elegans developmental timing. Cell 106, 23-34.
31. Hackler, L., Jr, Wan, J., Swaroop, A., Qian, J. and Zack, D. J. (2010). MicroRNA profile of the developing mouse retina. Invest. Ophthalmol. Vis. Sci. 51, 1823-1831.
32. Halfter, W., Willem, M. and Mayer, U. (2005). Basement membrane-dependent survival of retinal ganglion cells. Invest. Ophthalmol. Vis. Sci. 46, 1000-1009.
33. Halfter, W., Dong, S., Dong, A., Eller, A. W. and Nischt, R. (2008). Origin and turnover of ECM proteins from the inner limiting membrane and vitreous body. Eye 22, 1207-1213.
34. Harfe, B. D., McManus, M. T., Mansfield, J. H., Hornstein, E. and Tabin, C. J. (2005). The RNaseIII enzyme Dicer is required for morphogenesis but not patterning of the vertebrate limb. Proc. Natl. Acad. Sci. USA 102, 10898-10903.
35. Harris, K. S., Zhang, Z., Mcmanus, M. T., Harfe, B. D. and Sun, X. (2006). Dicer function is essential for lung epithelium morphogenesis. Proc. Natl. Acad. Sci. USA 103, 2208-2213.
36. Harvey, S. J., Jarad, G., Cunningham, J., Goldberg, S., Schermer, B., Harfe, B. D., McManus, M. T., Benzing, T. and Miner, J. H. (2008). Podocyte-specific deletion of dicer alters cytoskeletal dynamics and causes glomerular disease. J. Am. Soc. Nephrol. 19, 2150-2158.
37. Ho, J., Ng, K. H., Rosen, S., Dostal, A., Gregory, R. I. and Kreidberg, J. A. (2008). Podocyte-specific loss of functional microRNAs leads to rapid glomerular and tubular injury. J. Am. Soc. Nephrol. 19, 2069-2075.
38. Hornstein, E. and Shomron, N. (2006). Canalization of development by microRNAs. Nat. Genet. 38, S20-S24.
39. 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.
40. Inagaki, M., Irie, K., Ishizaki, H., Tanaka-Okamoto, M., Morimoto, K., Inoue, E., Ohtsuka, T., Miyoshi, J. and Takai, Y. (2005). Roles of cell-adhesion molecules nectin 1 and nectin 3 in ciliary body development. Development 132, 1525-1537.
41. Jadhav, A. P., Cho, S. H. and Cepko, C. L. (2006a). Notch activity permits retinal cells to progress through multiple progenitor states and acquire a stem cell property. Proc. Natl. Acad. Sci. USA 103, 18998-9003.
42. Jadhav, A. P., Mason, H. A. and Cepko, C. L. (2006b). Notch 1 inhibits photoreceptor production in the developing mammalian retina. Development 133, 913-923.
43. Kageyama, R. and Ohtsuka, T. (1999). The Notch-Hes pathway in mammalian neural development. Cell Res. 9, 179-188.
44. Kanellopoulou, C., Muljo, S. A., Kung, A. L., Ganesan, S., Drapkin, R., Jenuwein, T., Livingston, D. M. and Rajewsky, K. (2005). Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Genes Dev. 19, 489-501.
45. Karali, M., Peluso, I., Marigo, V. and Banfi, S. (2007). Identification and characterization of microRNAs expressed in the mouse eye. Invest. Ophthalmol. Vis. Sci. 48, 509-515.
46. Kogo, H., Ito, S. Y., Moritoki, Y., Kurahashi, H. and Fujimoto, T. (2006). Differential expression of caveolin-3 in mouse smooth muscle cells in vivo. Cell Tissue Res. 324, 291-300.
47. Larsen, K. B., Lutterodt, M., Rath, M. F. and Moller, M. (2009). Expression of the homeobox genes PAX6, OTX2, and OTX1 in the early human fetal retina. Int. J. Dev. Neurosci. 27, 485-492.
48. Lee, C. S., May, N. R. and Fan, C. M. (2001). Transdifferentiation of the ventral retinal pigmented epithelium to neural retina in the growth arrest specific gene 1 mutant. Dev. Biol. 236, 17-29.
49. Lee, R. C. and Ambros, V. (2001). An extensive class of small RNAs in Caenorhabditis elegans. Science 294, 862-864.
50. Li, S., Mo, Z., Yang, X., Price, S. M., Shen, M. M. and Xiang, M. (2004). Foxn4 controls the genesis of amacrine and horizontal cells by retinal progenitors. Neuron 43, 795-807.
51. Li, Y. and Piatigorsky, J. (2009). Targeted deletion of Dicer disrupts lens morphogenesis, corneal epithelium stratification, and whole eye development. Dev. Dyn. 238, 2388-2400.
52. Liu, H., Xu, S., Wang, Y., Mazerolle, C., Thurig, S., Coles, B. L., Ren, J. C., Taketo, M. M., Van Der Kooy, D. and Wallace, V. A. (2007). Ciliary margin transdifferentiation from neural retina is controlled by canonical Wnt signaling. Dev. Biol. 308, 54-67.
53. Lobe, C. G., Koop, K. E., Kreppner, W., Lomeli, H., Gertsenstein, M. and Nagy, A. (1999). Z/AP, a double reporter for cre-mediated recombination. Dev. Biol. 208, 281-292.
54. Maatouk, D. and Harfe, B. (2006). MicroRNAs in development. ScientificWorldJournal 6, 1828-1840.
55. Marquardt, T., Ashery-Padan, R., Andrejewski, N., Scardigli, R., Guillemot, F. and Gruss, P. (2001). Pax6 is required for the multipotent state of retinal progenitor cells. Cell 105, 43-55.
56. Martinez-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.
57. Melton, C., Judson, R. L. and Blelloch, R. (2010). Opposing microRNA families regulate self-renewal in mouse embryonic stem cells. Nature 463, 621-626
58. Mitashov, V. I. (2001). [Multipotent and stem cells in the developing, definitive, and regenerating vertebrate eye]. Izv. Akad. Nauk. Ser. Biol. 717-727.
59. Morrow, E. M., Furukawa, T., Lee, J. E. and Cepko, C. L. (1999). NeuroD regulates multiple functions in the developing neural retina in rodent. Development 126, 23-36.
60. Moshiri, A., Close, J. and Reh, T. A. (2004). Retinal stem cells and regeneration. Int. J. Dev. Biol. 48, 1003-1014.
61. Mu, X., Fu, X., Beremand, P. D., Thomas, T. L. and Klein, W. H. (2008). Gene regulation logic in retinal ganglion cell development: Isl1 defines a critical branch distinct from but overlapping with Pou4f2. Proc. Natl. Acad. Sci. USA 105, 6942-6947.
62. Napier, H. R. and Kidson, S. H. (2005). Proliferation and cell shape changes during ciliary body morphogenesis in the mouse. Dev. Dyn. 233, 213-223.
63. Parisi, M. J. and Lin, H. (1998). The role of the hedgehog/patched signaling pathway in epithelial stem cell proliferation: from fly to human. Cell Res. 8, 15-21.
64. Pasquinelli, A. E., Reinhart, B. J., Slack, F., Martindale, M. Q., Kuroda, M. I., Maller, B., Hayward, D. C., Ball, E. E., Degnan, B., Muller, P. et al. (2000). Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature 408, 86-89.
65. Reinhart, B. J., Slack, F. J., Basson, M., Pasquinelli, A. E., Bettinger, J. C., Rougvie, A. E., Horvitz, H. R. and Ruvkun, G. (2000). The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403, 901-906.
66. Riesenberg, A. N., Liu, Z., Kopan, R. and Brown, N. L. (2009). Rbpj cell autonomous regulation of retinal ganglion cell and cone photoreceptor fates in the mouse retina. J. Neurosci. 29, 12865-12877.
67. 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.
68. Ryan, D. G., Oliveira-Fernandes, M. and Lavker, R. M. (2006). MicroRNAs of the mammalian eye display distinct and overlapping tissue specificity. Mol. Vis. 12, 1175-1184.
69. Sage, C., Huang, M., Vollrath, M. A., Brown, M. C., Hinds, P. W., Corey, D. P., Vetter, D. E. and Chen, Z. Y. (2006). Essential role of retinoblastoma protein in mammalian hair cell development and hearing. Proc. Natl. Acad. Sci. USA 103, 7345-7350.
70. Sakagami, K., Gan, L. and Yang, X. J. (2009). Distinct effects of Hedgehog signaling on neuronal fate specification and cell cycle progression in the embryonic mouse retina. J. Neurosci. 29, 6932-6944.
71. Selbach, M., Schwanhausser, B., Thierfelder, N., Fang, Z., Khanin, R. and Rajewsky, N. (2008). Widespread changes in protein synthesis induced by microRNAs. Nature 455, 58-63.
72. Smith, R. S. (2002). Systematic Evaluation of the Mouse Eye. Boca Raton: CRC Press.
73. Spence, J. R., Madhavan, M., Ewing, J. D., Jones, D. K., Lehman, B. M. and Del Rio-Tsonis, K. (2004). The hedgehog pathway is a modulator of retina regeneration. Development 131, 4607-4621.
74. Strauss, O. (2005). The retinal pigment epithelium in visual function. Physiol. Rev. 85, 845-881.
75. Tropepe, V., Coles, B. L., Chiasson, B. J., Horsford, D. J., Elia, A. J., McInnes, R. R. and Van Der Kooy, D. (2000). Retinal stem cells in the adult mammalian eye. Science 287, 2032-2036.
76. Walther, C. and Gruss, P. (1991). Pax-6, a murine paired box gene, is expressed in the developing CNS. Development 113, 1435-1449.
77. Wang, F. E., Zhang, C., Maminishkis, A., Dong, L., Zhi, C., Li, R., Zhao, J., Majerciak, V., Gaur, A. B., Chen, S. et al. (2010). MicroRNA-204/211 alters epithelial physiology. FASEB J. 24, 1552-1571.
78. Wang, S. W., Kim, B. S., Ding, K., Wang, H., Sun, D., Johnson, R. L., Klein, W. H. and Gan, L. (2001). Requirement for math5 in the development of retinal ganglion cells. Genes Dev. 15, 24-29.
79. Wang, Y., Dakubo, G. D., Thurig, S., Mazerolle, C. J. and Wallace, V. A. (2005). Retinal ganglion cell-derived sonic hedgehog locally controls proliferation and the timing of RGC development in the embryonic mouse retina. Development 132, 5103-5113.
80. Wang, Y., Medvid, R., Melton, C., Jaenisch, R. and Blelloch, R. (2007). DGCR8 is essential for microRNA biogenesis and silencing of embryonic stem cell selfrenewal. Nat. Genet. 39, 380-385.
81. Wightman, B., Ha, I. and Ruvkun, G. (1993). Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 75, 855-862.
82. Xu, S., Witmer, P. D., Lumayag, S., Kovacs, B. and Valle, D. (2007). MicroRNA (miRNA) transcriptome of mouse retina and identification of a sensory organspecific miRNA cluster. J. Biol. Chem. 282, 25053-25066.
83. Yang, X. J. (2004). Roles of cell-extrinsic growth factors in vertebrate eye pattern formation and retinogenesis. Semin. Cell Dev. Biol. 15, 91-103.
84. Yaron, O., Farhy, C., Marquardt, T., Applebury, M. and Ashery-Padan, R. (2006). Notch1 functions to suppress cone-photoreceptor fate specification in the developing mouse retina. Development 133, 1367-1378.
85. Yi, R., Poy, M. N., Stoffel, M. and Fuchs, E. (2008). A skin microRNA promotes differentiation by repressing 'stemness'. Nature 452, 225-229.
86. Young, R. W. (1985). Cell differentiation in the retina of the mouse. Anat. Rec. 212, 199-205.
87. Yu, C., Mazerolle, C. J., Thurig, S., Wang, Y., Pacal, M., Bremner, R. and Wallace, V. A. (2006). Direct and indirect effects of hedgehog pathway activation in the mammalian retina. Mol. Cell. Neurosci. 32, 274-282.
88. Zhang, X. M. and Yang, X. J. (2001). Regulation of retinal ganglion cell production by Sonic hedgehog. Development 128, 943-957.
89. Zhao, S., Chen, Q., Hung, F. C. and Overbeek, P. A. (2002). BMP signaling is required for development of the ciliary body. Development 129, 4435-4442.