Lens and retina regeneration: New perspectives from model organisms

Biochemical Journal

Volumn 447, Issue 3, 2012, Pages 321-334

  Barbosa Sabanero, Karla ^a   Hoffmann, Andrea ^b   Judge, Chelsey ^a   Lightcap, Nicole ^a   Tsonis, Panagiotis A ^b   Del Rio Tsonis, K ^a  

^a MIAMI UNIVERSITY   (United States)

^b UNIVERSITY OF DAYTON   (United States)

Author keywords

Lens; Model organism; Regeneration; Retina

Indexed keywords

ALPHA CRYSTALLIN; BETA CRYSTALLIN; BONE MORPHOGENETIC PROTEIN; FIBROBLAST GROWTH FACTOR; GAMMA CRYSTALLIN; MITOGEN ACTIVATED PROTEIN KINASE; WNT PROTEIN;

AMPHIBIA; ANATOMY; BIRD; CELL GROWTH; CELL TRANSDIFFERENTIATION; CILIARY BODY; CORNEA LENS TRANSDIFFERENTIATION; EPIGENETICS; EXTRACELLULAR MATRIX; FISH; LENS REGENERATION; MAMMAL; MOLECULAR DYNAMICS; MUELLER CELL; NONHUMAN; PHYSIOLOGY; PRIORITY JOURNAL; REVIEW; SALAMANDRIDAE; STEM CELL; TISSUE REGENERATION; VISUAL PIGMENT REGENERATION; WNT SIGNALING PATHWAY; XENOPUS;

AMPHIBIANS; ANIMALS; HUMANS; LENS, CRYSTALLINE; MAMMALS; MODELS, ANIMAL; REGENERATION; RETINA; SPECIES SPECIFICITY;

EID: 84867242963     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20120813     Document Type: Review

References (187)

1. Wolff, G. (1895) Entwicklungsphyiologische Studien. I. Die Regeneration der Urodelenlinse. Wilhelm Roux' Arch. Entwicklungsmech. Org. 1, 380-390
2. Colluci, V. (1891) Sulla rigenerazione parziale deell'occhio nei tritoni: isogenesi esvilluppo-Studio seprimentale. Mem. Accad. Sci. Ist. Bologna, Cl. Sci. Fis. 5, 593-621
3. Eguchi, G., Eguchi, Y., Nakamura, K., Yadav, M. C., Millan, J. L. and Tsonis, P. A. (2011) Regenerative capacity in newts is not altered by repeated regeneration and ageing. Nat. Commun. 2, 384
4. Kuszak, J. R., Zoltoski, R. K. and Sivertson, C. (2004) Fibre cell organization in crystalline lenses. Exp. Eye Res. 78, 673-687 (Pubitemid 38183346)
5. Kuszak, J. R., Mazurkiewicz, M., Jison, L., Madurski, A., Ngando, A. and Zoltoski, R. K. (2006) Quantitative analysis of animal model lens anatomy: accommodative range is related to fiber structure and organization. Vet. Ophthalmol. 9, 266-280 (Pubitemid 44290203)
6. Al-Ghoul, K. J., Kuszak, J. R., Lu, J. Y. and Owens, M. J. (2003) Morphology and organization of posterior fiber ends during migration. Mol. Vision 9, 119-128 (Pubitemid 38097576)
7. Henry, J. J. (2003) The cellular and molecular bases of vertebrate lens regeneration. Int. Rev. Cytol. 228, 195-265
8. Filoni, S. (2009) Retina and lens regeneration in anuran amphibians. Semin. Cell Dev. Biol. 20, 528-534
9. Freeman, G. (1963) Lens regeneration from the cornea in Xenopus laevis. J. Exp. Zool. 154, 39-65
10. Henry, J. J. and Elkins, M. B. (2001) Cornea-lens transdifferentiation in the anuran, Xenopus tropicalis. Dev. Genes Evol. 211, 377-387 (Pubitemid 32927033)
11. Filoni, S., Bernardini, S. and Cannata, S. M. (2006) Experimental analysis of lens-forming capacity in Xenopus borealis larvae. J. Exp. Zool., Part A 305, 538-550 (Pubitemid 44049324)
12. 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 (Pubitemid 46241111)
13. Piatigorsky, J. (1992) Lens crystallins: innovation associated with changes in gene regulation. J. Biol. Chem. 267, 4277-4280
14. Mizuno, N., Mochii, M., Takahashi, T. C., Eguchi, G. and Okada, T. S. (1999) Lens regeneration in Xenopus is not a mere repeat of lens development, with respect to crystallin gene expression. Differentiation 64, 143-149 (Pubitemid 29213880)
15. Brahma, S. K. and McDevitt, D. S. (1974) Ontogeny and localization of the lens crystallins in Xenopus laevis lens regeneration. J. Embryol. Exp. Morphol. 32, 783-794
16. Campbell, J. C. and Truman, D. E. (1977) Variations in differentiation in the regenerating lens of Xenopus laevis. Exp. Eye Res. 25, 99-100
17. Day, R. C. and Beck, C. W. (2011) Transdifferentiation from cornea to lens in Xenopus laevis depends on BMP signalling and involves upregulation of Wnt signalling. BMC Dev. Biol. 11, 54
18. Filoni, S., Bosco, L. and Cioni, C. (1982) The role of neural retina in lens regeneration from cornea in larval Xenopus laevis. Acta Embryol. Morphol. Exp. 3, 15-28 (Pubitemid 13125684)
19. Reeve, J. G. and Wild, A. E. (1981) Secondary lens formation from the cornea following implantation of larval tissues between the inner and outer corneas of Xenopus laevis tadpoles. J. Embryol. Exp. Morphol. 64, 121-132 (Pubitemid 11039714)
20. Bosco, L., Testa, O., Venturini, G. and Willems, D. (1997) Lens fibre transdifferentiation in cultured larval Xenopus laevis outer cornea under the influence of neural retina-conditioned medium. Cell. Mol. Life Sci. 53, 921-928 (Pubitemid 28021506)
21. Fukui, L. and Henry, J. J. (2011) FGF signaling is required for lens regeneration in Xenopus laevis. Biol. Bull. 221, 137-145
22. Bosco, L., Venturini, G. and Willems, D. (1997) In vitro lens transdifferentiation of Xenopus laevis outer cornea induced by fibroblast growth factor (FGF). Development 124, 421-428 (Pubitemid 27101676)
23. Arresta, E., Bernardini, S., Gargioli, C., Filoni, S. and Cannata, S. M. (2005) Lens-forming competence in the epidermis of Xenopus laevis during development. J. Exp. Zool., Part A 303, 1-12 (Pubitemid 40118349)
24. Henry, J. J., Carinato, M. E., Schaefer, J. J., Wolfe, A. D., Walter, B. E., Perry, K. J. and Elbl, T. N. (2002) Characterizing gene expression during lens formation in Xenopus laevis: evaluating the model for embryonic lens induction. Dev. Dyn. 224, 168-185 (Pubitemid 34569058)
25. Schaefer, J. J., Oliver, G. and Henry, J. J. (1999) Conservation of gene expression during embryonic lens formation and cornea-lens transdifferentiation in Xenopus laevis. Dev. Dyn. 215, 308-318 (Pubitemid 29377200)
26. Malloch, E. L., Perry, K. J., Fukui, L., Johnson, V. R., Wever, J., Beck, C. W., King, M. W. and Henry, J. J. (2009) Gene expression profiles of lens regeneration and development in Xenopus laevis. Dev. Dyn. 238, 2340-2356
27. Gargioli, C., Giambra, V., Santoni, S., Bernardini, S., Frezza, D., Filoni, S. and Cannata, S. M. (2008) The lens-regenerating competence in the outer cornea and epidermis of larval Xenopus laevis is related to pax6 expression. J. Anat. 212, 612-620 (Pubitemid 351593966)
28. Mizuno, N., Mochii, M., Yamamoto, T. S., Takahashi, T. C., Eguchi, G. and Okada, T. S. (1999) Pax-6 and Prox 1 expression during lens regeneration from Cynops iris and Xenopus cornea: evidence for a genetic program common to embryonic lens development. Differentiation 65, 141-149
29. Zygar, C. A., Cook, T. L. and Grainger, Jr, R. M. (1998) Gene activation during early stages of lens induction in Xenopus. Development 125, 3509-3519 (Pubitemid 28458349)
30. Cvekl, A. and Piatigorsky, J. (1996) Lens development and crystallin gene expression: many roles for Pax-6. BioEssays 18, 621-630 (Pubitemid 26311999)
31. Mizuno, N., Ueda, Y. and Kondoh, H. (2005) Requirement for β B1-crystallin promoter of Xenopus laevis in embryonic lens development and lens regeneration. Dev. Growth Differ. 47, 131-140 (Pubitemid 40676935)
32. Ogino, H., Fisher, M. and Grainger, R. M. (2008) Convergence of a head-field selector Otx2 and Notch signaling: a mechanism for lens specification. Development 135, 249-258 (Pubitemid 351228417)
33. Carinato, M. E., Walter, B. E. and Henry, J. J. (2000) Xenopus laevis gelatinase B (Xmmp-9): development, regeneration, and wound healing. Dev. Dyn. 217, 377-387 (Pubitemid 30185561)
34. Perry, K. J., Johnson, V. R., Malloch, E. L., Fukui, L., Wever, J., Thomas, A. G., Hamilton, P. W. and Henry, J. J. (2010) The G-protein-coupled receptor, GPR84, is important for eye development in Xenopus laevis. Dev. Dyn. 239, 3024-3037
35. Stone, L. S. (1957) Further experiments on lens regeneration from retina pigment cells in adult newt eyes. J. Exp. Zool. 136, 75-87
36. Stone, L. S. (1953) An experimental analysis of lens regeneration. Am. J. Ophthalmol. 36, 31-39
37. Eguchi, G. and Shingai, R. (1971) Cellular analysis on localization of lens forming potency in the newt iris epithelium. Dev. Growth Differ. 13, 337-349
38. Reyer, R. W., Woolfitt, R. A. and Withersty, L. T. (1973) Stimulation of lens regeneration from the newt dorsal iris when implanted into the blastema of the regenerating limb. Dev. Biol. 32, 258-281
39. Reyer, R. W. (1977) Repolarization of reversed, regenerating lenses in adult newts, Notophthalmus viridescens. Exp. Eye Res. 24, 501-509
40. Yamada, T. (1977) Control mechanisms in cell-type conversion in newt lens regeneration. Monogr. Dev. Biol. 13, 1-126
41. Eguchi, G. (1963) Electron microscopic studies on lens regeneration. 1. Mechanism of depigmentation of iris. Embryologia 8, 45-62
42. Eguchi, G. (1964) Electiron microscopic studies on lens regeneration II. Formation and growth of lens vesicle and differentiation of lens fibers. Embryologia 8, 247-287
43. Ito, M., Hayashi, T., Kuroiwa, A. and Okamoto, M. (1999) Lens formation by pigmented epithelial cell reaggregate from dorsal iris implanted into limb blastema in the adult newt. Dev. Growth Differ. 41, 429-440 (Pubitemid 29369935)
44. Grogg, M. W., Call, M. K., Okamoto, M., Vergara, M. N., Del Rio-Tsonis, K. and Tsonis, P. A. (2005) BMP inhibition-driven regulation of six-3 underlies induction of newt lens regeneration. Nature 438, 858-862 (Pubitemid 41753068)
45. Eguchi, G., Abe, S. I. and Watanabe, K. (1974) Differentiation of lens-like structures from newt iris epithelial cells in vitro. Proc. Natl. Acad. Sci. U.S.A. 71, 5052-5056
46. Mizuno, N., Agata, K., Sawada, K., Mochii, M. and Eguchi, G. (2002) Expression of crystallin genes in embryonic and regenerating newt lenses. Dev. Growth Differ. 44, 251-256
47. McDevitt, D. S., Brahma, S. K., Courtois, Y. and Jeanny, J. C. (1997) Fibroblast growth factor receptors and regeneration of the eye lens. Dev. Dyn. 208, 220-226 (Pubitemid 27068877)
48. Del Rio-Tsonis, K., Trombley, M. T., McMahon, G. and Tsonis, P. A. (1998) Regulation of lens regeneration by fibroblast growth factor receptor 1. Dev. Dyn. 213, 140-146 (Pubitemid 28394916)
49. Hayashi, T., Mizuno, N., Ueda, Y., Okamoto, M. and Kondoh, H. (2004) FGF2 triggers iris-derived lens regeneration in newt eye. Mech. Dev. 121, 519-526 (Pubitemid 38681207)
50. Madhavan, M., Haynes, T. L., Frisch, N. C., Call, M. K., Minich, C. M., Tsonis, P. A. and Del Rio-Tsonis, K. (2006) The role of Pax-6 in lens regeneration. Proc. Natl. Acad. Sci. U.S.A. 103, 14848-14853 (Pubitemid 44527817)
51. Del Rio-Tsonis, K., Washabaugh, C. H. and Tsonis, P. A. (1995) Expression of pax-6 during urodele eye development and lens regeneration. Proc. Natl. Acad. Sci. U.S.A. 92, 5092-5096
52. Markitantova, Y. V., Makariev, E. O., Pavlova, G. V., Zinovieva, R. D. and Mitashov, V. I. (2003) Location of the Prox1 gene expression during newt lens and retina regeneration. Dokl. Biol. Sci. 391, 361-364
53. Del Rio-Tsonis, K., Tomarev, S. I. and Tsonis, P. A. (1999) Regulation of Prox1 during lens regeneration. Invest. Ophthalmol. Visual Sci. 40, 2039-2045
54. Hayashi, T., Mizuno, N., Takada, R., Takada, S. and Kondoh, H. (2006) Determinative role of Wnt signals in dorsal iris-derived lens regeneration in newt eye. Mech. Dev. 123, 793-800 (Pubitemid 44709505)
55. Tsonis, P. A., Vergara, M. N., Spence, J. R., Madhavan, M., Kramer, E. L., Call, M. K., Santiago, W. G., Vallance, J. E., Robbins, D. J. and Del Rio-Tsonis, K. (2004) A novel role of the hedgehog pathway in lens regeneration. Dev. Biol. 267, 450-461 (Pubitemid 38328584)
56. Maki, N., Martinson, J., Nishimura, O., Tarui, H., Meller, J., Tsonis, P. A. and Agata, K. (2010) Expression profiles during dedifferentiation in newt lens regeneration revealed by expressed sequence tags. Mol. Vision 16, 72-78
57. Kulyk, W. M. and Zalik, S. E. (1982) Synthesis of sulfated glycosaminoglycan in newt iris during lens regeneration. Differentiation 23, 29-35 (Pubitemid 13178259)
58. Kulyk, W. M., Zalik, S. E. and Dimitrov, E. (1987) Hyaluronic acid production and hyaluronidase activity in the newt iris during lens regeneration. Exp. Cell Res. 172, 180-191
59. Makarev, E., Call, M. K., Grogg, M. W., Atkinson, D. L., Milash, B., Odelberg, S. J. and Tsonis, P. A. (2007) Gene expression signatures in the newt irises during lens regeneration. FEBS Lett. 581, 1865-1870 (Pubitemid 46602283)
60. Elgert, K. L. and Zalik, S. E. (1989) Fibronectin distribution during cell type conversion in newt lens regeneration. Anat. Embryol. 180, 131-142
61. Godwin, J. W., Liem, Jr, K. F. and Brockes, J. P. (2010) Tissue factor expression in newt iris coincides with thrombin activation and lens regeneration. Mech. Dev. 127, 321-328
62. Imokawa, Y., Simon, A. and Brockes, J. P. (2004) A critical role for thrombin in vertebrate lens regeneration. Philos. Trans. R. Soc. London Ser. B 359, 765-776 (Pubitemid 38673744)
63. Imokawa, Y. and Brockes, J. P. (2003) Selective activation of thrombin is a critical determinant for vertebrate lens regeneration. Curr. Biol. 13, 877-881 (Pubitemid 36573258)
64. Hayashi, T., Mizuno, N. and Kondoh, H. (2008) Determinative roles of FGF and Wnt signals in iris-derived lens regeneration in newt eye. Dev. Growth Differ. 50, 279-287 (Pubitemid 351661155)
65. Maki, N., Suetsugu-Maki, R., Sano, S., Nakamura, K., Nishimura, O., Tarui, H., Del Rio-Tsonis, K., Ohsumi, K., Agata, K. and Tsonis, P. A. (2010) Oocyte-type linker histone B4 is required for transdifferentiation of somatic cells in vivo. FASEB J. 24, 3462-3467
66. Maki, N., Tsonis, P. A. and Agata, K. (2010) Changes in global histone modifications during dedifferentiation in newt lens regeneration. Mol. Vision 16, 1893-1897
67. Maki, N., Takechi, K., Sano, S., Tarui, H., Sasai, Y. and Agata, K. (2007) Rapid accumulation of nucleostemin in nucleolus during newt regeneration. Dev. Dyn. 236, 941-950 (Pubitemid 46641335)
68. Takahashi, K. and Yamanaka, S. (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663-676 (Pubitemid 44233629)
69. Maki, N., Suetsugu-Maki, R., Tarui, H., Agata, K., Del Rio-Tsonis, K. and Tsonis, P. A. (2009) Expression of stem cell pluripotency factors during regeneration in newts. Dev. Dyn. 238, 1613-1616
70. Makarev, E., Spence, J. R., Del Rio-Tsonis, K. and Tsonis, P. A. (2006) Identification of microRNAs and other small RNAs from the adult newt eye. Mol. Vision 12, 1386-1391 (Pubitemid 44835131)
71. Tsonis, P. A., Call, M. K., Grogg, M. W., Sartor, M. A., Taylor, R. R., Forge, A., Fyffe, R., Goldenberg, R., Cowper-Sal-lari, R. and Tomlinson, C. R. (2007) MicroRNAs and regeneration: Let-7 members as potential regulators of dedifferentiation in lens and inner ear hair cell regeneration of the adult newt. Biochem. Biophys. Res. Commun. 362, 940-945 (Pubitemid 47398872)
72. Nakamura, K., Maki, N., Trinh, A., Trask, H. W., Gui, J., Tomlinson, C. R. and Tsonis, P. A. (2010) miRNAs in newt lens regeneration: specific control of proliferation and evidence for miRNA networking. PLoS ONE 5, e12058
73. Cocteau, M. M. and D'Etoille, L. (1827) Reproduction du crystallin. J. Physiol. Exp. Pathol. 1, 730-744
74. Kessler, J. (1975) Lens refilling and regrowth of lens substance in the rabbit eye. Ann. Ophthalmol. 7, 1059-1062
75. Gwon, A., Enomoto, H., Horowitz, J. and Garner, M. H. (1989) Induction of de novo synthesis of crystalline lenses in aphakic rabbits. Exp. Eye Res. 49, 913-926 (Pubitemid 20043704)
76. Gwon, A. E., Gruber, L. J. and Mundwiler, K. E. (1990) A histologic study of lens regeneration in aphakic rabbits. Invest. Ophthalmol. Visual Sci. 31, 540-547 (Pubitemid 20117072)
77. Gwon, A. E., Jones, R. L., Gruber, L. J. and Mantras, C. (1992) Lens regeneration in juvenile and adult rabbits measured by image analysis. Invest. Ophthalmol. Visual Sci. 33, 2279-2283
78. Call, M. K., Grogg, M. W., Del Rio-Tsonis, K. and Tsonis, P. A. (2004) Lens regeneration in mice: implications in cataracts. Exp. Eye Res. 78, 297-299 (Pubitemid 38077234)
79. Huang, Y. and Xie, L. (2010) Expression of transcription factors and crystallin proteins during rat lens regeneration. Mol. Vision 16, 341-352
80. Randolph, R. L. (1900) The regeneration of the crystallin lens: an experimental study. Johns Hopkins Hosp. Rep. 9, 237-263
81. Medvedovic, M., Tomlinson, C. R., Call, M. K., Grogg, M. and Tsonis, P. A. (2006) Gene expression and discovery during lens regeneration in mouse: regulation of epithelial to mesenchymal transition and lens differentiation. Mol. Vision 12, 422-440
82. Lois, N., Reid, B., Song, B., Zhao, M., Forrester, J. and McCaig, C. (2010) Electric currents and lens regeneration in the rat. Exp. Eye Res. 90, 316-323
83. Griffini, L. and Marcchio, G. (1889) Sulla rigenerazione totale della retina nei tritoni. Riforma Med. 5, 86-93
84. Del Rio-Tsonis, K. and Tsonis, P. A. (2003) Eye regeneration at the molecular age. Dev. Dyn. 226, 211-224 (Pubitemid 36163338)
85. Haynes, T. and Del Rio-Tsonis, K. (2004) Retina repair, stem cells and beyond. Curr. Neurovasc. Res. 1, 231-239
86. Zhu, J., Zhang, E. and Del Rio-Tsonis, K. (2012) Eye Anatomy. eLS, John Wiley & Sons Ltd, Chichester; http://www.els.net, doi:10.1002/9780470015902. a0000108.pub2
87. Steinberg, R. H. (1985) Interactions between the retinal-pigment epithelium and the neural retina. Doc. Ophthalmol. 60, 327-346
88. Strauss, O. (2005) The retinal pigment epithelium in visual function. Physiol. Rev. 85, 845-881
89. 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 (Pubitemid 46399687)
90. Locker, M., El Yakoubi, W., Mazurier, N., Dullin, J. P. and Perron, M. (2010) A decade of mammalian retinal stem cell research. Arch. Ital. Biol. 148, 59-72
91. Perron, M., Kanekar, S., Vetter, M. L. and Harris, W. A. (1998) The genetic sequence of retinal development in the ciliary margin of the Xenopus eye. Dev. Biol. 199, 185-200 (Pubitemid 28364200)
92. Wetts, R., Serbedzija, G. N. and Fraser, S. E. (1989) Cell lineage analysis reveals multipotent precursors in the ciliary margin of the frog retina. Dev. Biol. 136, 254-263 (Pubitemid 19262701)
93. Hollyfield, J. G. (1968) Differential addition of cells to the retina in Rana pipiens tadpoles. Dev. Biol. 18, 163-179
94. Johns, P. R. (1977) Growth of the adult goldfish eye. III. Source of the new retinal cells. J. Comp. Neurol. 176, 343-357
95. Johns, P. R. and Easter, Jr, S. S. (1977) Growth of the adult goldfish eye. II. Increase in retinal cell number. J. Comp. Neurol. 176, 331-341 (Pubitemid 8224347)
96. Lyall, A. H. (1957) The growth of the trout retina. Q. J. Microsc. Sci. 98, 101-110
97. Straznicky, K. and Gaze, R. M. (1971) The growth of the retina in Xenopus laevis: an autoradiographic study. J. Embryol. Exp. Morphol. 26, 67-79
98. Bernardos, R. L., Barthel, L. K., Meyers, J. R. and Raymond, P. A. (2007) Late-stage neuronal progenitors in the retina are radial Müller glia that function as retinal stem cells. J. Neurosci. 27, 7028-7040 (Pubitemid 47015895)
99. Johns, P. R. and Fernald, R. D. (1981) Genesis of rods in teleost fish retina. Nature 293, 141-142 (Pubitemid 11009897)
100. Raymond, P. A., Barthel, L. K., Bernardos, R. L. and Perkowski, J. J. (2006) Molecular characterization of retinal stem cells and their niches in adult zebrafish. BMC Dev. Biol. 6, 36
101. Hitchcock, P., Ochocinska, M., Sieh, A. and Otteson, D. (2004) Persistent and injury-induced neurogenesis in the vertebrate retina. Prog. Retinal Eye Res. 23, 183-194 (Pubitemid 38496400)
102. Mitashov, V. I. (1968) [Autoradiographic study of the retinal regeneration in the newt (Triturus cristatus)]. Dokl. Akad. Nauk SSSR 181, 1510-1513
103. Reh, T. A. (1987) Cell-specific regulation of neuronal production in the larval frog retina. J. Neurosci. 7, 3317-3324
104. Reh, T. A. and Nagy, T. (1987) A possible role for the vascular membrane in retinal regeneration in Rana catesbienna tadpoles. Dev. Biol. 122, 471-482
105. Reyer, R. W. (1971) The origins of the regenerating neural retina in two species of urodele. Anat. Rec. 169, 410-411
106. Stenkamp, D. L., Powers, M. K., Carney, L. H. and Cameron, D. A. (2001) Evidence for two distinct mechanisms of neurogenesis and cellular pattern formation in regenerated goldfish retinas. J. Comp. Neurol. 431, 363-381 (Pubitemid 32178942)
107. Araki, M. (2007) Regeneration of the amphibian retina: role of tissue interaction and related signaling molecules on RPE transdifferentiation. Dev. Growth Differ. 49, 109-120
108. 1 tubulin-expressing Müller glia in regeneration of the injured zebrafish retina. J. Neurosci. 26, 6303-6313
109. Stenkamp, D. L. (2007) Neurogenesis in the fish retina. Int. Rev. Cytol. 259, 173-224
110. Thummel, R., Kassen, S. C., Enright, J. M., Nelson, C. M., Montgomery, J. E. and Hyde, D. R. (2008) Characterization of Müller glia and neuronal progenitors during adult zebrafish retinal regeneration. Exp. Eye Res. 87, 433-444
111. Martinez-De Luna, R. I., Kelly, L. E. and El-Hodiri, H. M. (2011) The retinal homeobox (Rx) gene is necessary for retinal regeneration. Dev. Biol. 353, 10-18
112. 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 (Pubitemid 30228147)
113. Moshiri, A., McGuire, C. R. and Reh, T. A. (2005) Sonic hedgehog regulates proliferation of the retinal ciliary marginal zone in posthatch chicks. Dev. Dyn. 233, 66-75 (Pubitemid 40548024)
114. Fischer, A. J. and Reh, T. A. (2003) Growth factors induce neurogenesis in the ciliary body. Dev. Biol. 259, 225-240 (Pubitemid 36836142)
115. 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
116. Coulombre, J. L. and Coulombre, A. J. (1970) Influence of mouse neural retina on regeneration of chick neural retina from chick embryonic pigmented epithelium. Nature 228, 559-560
117. Park, C. M. and Hollenberg, M. J. (1991) Induction of retinal regeneration in vivo by growth factors. Dev. Biol. 148, 322-333 (Pubitemid 121004771)
118. Spence, J. R., Aycinena, J. C. and Del Rio-Tsonis, K. (2007) Fibroblast growth factor-hedgehog interdependence during retina regeneration. Dev. Dyn. 236, 1161-1174 (Pubitemid 46750250)
119. 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 (Pubitemid 39409700)
120. Ghai, K., Stanke, J. J. and Fischer, A. J. (2008) Patterning of the circumferential marginal zone of progenitors in the chicken retina. Brain Res. 1192, 76-89 (Pubitemid 351199477)
121. Venters, S. J., Cuenca, P. D. and Hyer, J. (2011) Retinal and anterior eye compartments derive from a common progenitor pool in the avian optic cup. Mol. Vision 17, 3347-3363
122. Haynes, T., Gutierrez, C., Aycinena, J. C., Tsonis, P. A. and Del Rio-Tsonis, K. (2007) BMP signaling mediates stem/progenitor cell-induced retina regeneration. Proc. Natl. Acad. Sci. U.S.A. 104, 20380-20385
123. Lopashov, G. V. and Sologub, A. A. (1972) Artificial metaplasia of pigmented epithelium into retina in tadpoles and adult frogs. J. Embryol. Exp. Morphol. 28, 521-546
124. Vergara, M. N. and Del Rio-Tsonis, K. (2009) Retinal regeneration in the Xenopus laevis tadpole: a new model system. Mol. Vision 15, 1000-1013
125. Reh, T. A., Nagy, T. and Gretton, H. (1987) Retinal pigmented epithelial cells induced to transdifferentiate to neurons by laminin. Nature 330, 68-71 (Pubitemid 17152415)
126. Ueda, Y., Mizuno, N. and Araki, M. (2012) Transgenic Xenopus laevis with the ef1-α promoter as an experimental tool for amphibian retinal regeneration study. Genesis 50, 642-650
127. Kuriyama, F., Ueda, Y. and Araki, M. (2009) Complete reconstruction of the retinal laminar structure from a cultured retinal pigment epithelium is triggered by altered tissue interaction and promoted by overlaid extracellular matrices. Dev. Neurobiol. 69, 950-958
128. Chiba, C. and Mitashov, V. I. (2007) Cellular and molecular events in the adult newt retinal regeneration. In Strategies for Retinal Tissue Repair and Regeneration in Vertebrates: From Fish to Human (Chiba, C., ed.), pp. 15- 33, Research Signpost, Trivandrum
129. Saito, T., Kaneko, Y., Maruo, F., Niino, M. and Sakaki, Y. (1994) Study of the regenerating newt retina by electrophysiology and immunohistochemistry (bipolar- and cone-specific antigen localization). J. Exp. Zool. 270, 491-500
130. Chiba, C., Oi, H. and Saito, T. (2005) Changes in somatic sodium currents of ganglion cells during retinal regeneration in the adult newt. Dev. Brain Res. 154, 25-34 (Pubitemid 40023127)
131. Kaneko, Y. and Saito, T. (1992) Appearance and maturation of voltage-dependent conductances in solitary spiking cells during retinal regeneration in the adult newt. J. Comp. Physiol., A 170, 411-425
132. Chiba, C., Matsushima, O., Muneoka, Y. and Saito, T. (1997) Time course of appearance of GABA and GABA receptors during retinal regeneration in the adult newt. Dev. Brain Res. 98, 204-210 (Pubitemid 27075276)
133. Chiba, C., Hoshino, A., Nakamura, K., Susaki, K., Yamano, Y., Kaneko, Y., Kuwata, O., Maruo, F. and Saito, T. (2006) Visual cycle protein RPE65 persists in new retinal cells during retinal regeneration of adult newt. J. Comp. Neurol. 495, 391-407 (Pubitemid 43375813)
134. Kaneko, Y., Matsumoto, G. and Hanyu, Y. (1999) Pax-6 expression during retinal regeneration in the adult newt. Dev. Growth Differ. 41, 723-729 (Pubitemid 30026669)
135. Nakamura, K. and Chiba, C. (2007) Evidence for Notch signaling involvement in retinal regeneration of adult newt. Brain Res. 1136, 28-42 (Pubitemid 46209085)
136. Sakami, S., Hisatomi, O., Sakakibara, S., Liu, J., Reh, T. A. and Tokunaga, F. (2005) Downregulation of Otx2 in the dedifferentiated RPE cells of regenerating newt retina. Dev. Brain Res. 155, 49-59 (Pubitemid 40347308)
137. Susaki, K., Kaneko, J., Yamano, Y., Nakamura, K., Inami, W., Yoshikawa, T., Ozawa, Y., Shibata, S., Matsuzaki, O., Okano, H. and Chiba, C. (2009) Musashi-1, an RNA-binding protein, is indispensable for survival of photoreceptors. Exp. Eye Res. 88, 347-355
138. Kaneko, J. and Chiba, C. (2009) Immunohistochemical analysis of Musashi-1 expression during retinal regeneration of adult newt. Neurosci. Lett. 450, 252-257
139. Cheon, E. W., Kaneko, Y. and Saito, T. (1998) Regeneration of the newt retina: order of appearance of photoreceptors and ganglion cells. J. Comp. Neurol. 396, 267-274 (Pubitemid 28249176)
140. + ATPase is up-regulated in dedifferentiated progenitor cells that mediate lens and retina regeneration in adult newts. Exp. Eye Res. 88, 314-322
141. Susaki, K. and Chiba, C. (2007) MEK mediates in vitro neural transdifferentiation of the adult newt retinal pigment epithelium cells: is FGF2 an induction factor? Pigm. Cell Res. 20, 364-379 (Pubitemid 47390121)
142. Yoshikawa, T., Mizuno, A., Yasumuro, H., Inami, W., Vergara, M. N., Rio-Tsonis, K. D. and Chiba, C. (2012) MEK-ERK and heparin-susceptible signaling pathways are involved in cell-cycle entry of the wound edge retinal pigment epithelium cells in the adult newt. Pigm. Cell Melanoma Res. 25, 66-82
143. Ikegami, Y., Mitsuda, S. and Araki, M. (2002) Neural cell differentiation from retinal pigment epithelial cells of the newt: an organ culture model for the urodele retinal regeneration. J. Neurobiol. 50, 209-220 (Pubitemid 34131052)
144. Mitsuda, S., Yoshii, C., Ikegami, Y. and Araki, M. (2005) Tissue interaction between the retinal pigment epithelium and the choroid triggers retinal regeneration of the newt Cynops pyrrhogaster. Dev. Biol. 280, 122-132 (Pubitemid 40342747)
145. Park, C. M. and Hollenberg, M. J. (1989) Basic fibroblast growth factor induces retinal regeneration in vivo. Dev. Biol. 134, 201-205 (Pubitemid 19176481)
146. Park, C. M. and Hollenberg, M. J. (1993) Growth factor-induced retinal regeneration in vivo. Int. Rev. Cytol. 146, 49-74 (Pubitemid 23286699)
147. Spence, J. R., Madhavan, M., Aycinena, J. C. and Del Rio-Tsonis, K. (2007) Retina regeneration in the chick embryo is not induced by spontaneous Mitf downregulation but requires FGF/FGFR/MEK/Erk dependent upregulation of Pax6. Mol. Vision 13, 57-65 (Pubitemid 46158157)
148. Sakami, S., Etter, P. and Reh, T. A. (2008) Activin signaling limits the competence for retinal regeneration from the pigmented epithelium. Mech. Dev. 125, 106-116 (Pubitemid 350299132)
149. Toy, J., Yang, J. M., Leppert, G. S. and Sundin, O. H. (1998) The optx2 homeobox gene is expressed in early precursors of the eye and activates retina-specific genes. Proc. Natl. Acad. Sci. U.S.A. 95, 10643-10648 (Pubitemid 28413121)
150. Wang, S. Z., Ma, W., Yan, R. T. and Mao, W. (2010) Generating retinal neurons by reprogramming retinal pigment epithelial cells. Expert Opin. Biol. Ther. 10, 1227-1239
151. Yan, R. T., Liang, L., Ma, W., Li, X., Xie, W. and Wang, S. Z. (2010) Neurogenin1 effectively reprograms cultured chick retinal pigment epithelial cells to differentiate toward photoreceptors. J. Comp. Neurol. 518, 526-546
152. Kawasaki, A., Otori, Y. and Barnstable, C. J. (2000) Müller cell protection of rat retinal ganglion cells from glutamate and nitric oxide neurotoxicity. Invest. Ophthalmol. Visual Sci. 41, 3444-3450
153. Hollander, H., Makarov, F., Dreher, Z., van Driel, D., Chan-Ling, T. L. and Stone, J. (1991) Structure of the macroglia of the retina: sharing and division of labour between astrocytes and Müller cells. J. Comp. Neurol. 313, 587-603
154. Forrester, J. V., Liversidge, J. and Dua, H. S. (1990) Regulation of the local immune response by retinal cells. Curr. Eye Res. 9 (Suppl.), 183-191 (Pubitemid 20295621)
155. Roberge, F. G., Caspi, R. R. and Nussenblatt, R. B. (1988) Glial retinal Müller cells produce IL-1 activity and have a dual effect on autoimmune T helper lymphocytes: antigen presentation manifested after removal of suppressive activity. J. Immunol. 140, 2193-2196 (Pubitemid 18098474)
156. Faillace, M. P., Julian, D. and Korenbrot, J. I. (2002) Mitotic activation of proliferative cells in the inner nuclear layer of the mature fish retina: regulatory signals and molecular markers. J. Comp. Neurol. 451, 127-141 (Pubitemid 34920405)
157. Kassen, S. C., Thummel, R., Burket, C. T., Campochiaro, L. A., Harding, M. J. and Hyde, D. R. (2008) The Tg(ccnb1:EGFP) transgenic zebrafish line labels proliferating cells during retinal development and regeneration. Mol. Vision 14, 951-963 (Pubitemid 351784317)
158. Yurco, P. and Cameron, D. A. (2005) Responses of Müller glia to retinal injury in adult zebrafish. Vision Res. 45, 991-1002 (Pubitemid 40203370)
159. Wu, D. M., Schneiderman, T., Burgett, J., Gokhale, P., Barthel, L. and Raymond, P. A. (2001) Cones regenerate from retinal stem cells sequestered in the inner nuclear layer of adult goldfish retina. Invest. Ophthalmol. Visual Sci. 42, 2115-2124 (Pubitemid 32726047)
160. Brockerhoff, S. E. and Fadool, J. M. (2011) Genetics of photoreceptor degeneration and regeneration in zebrafish. Cell. Mol. Life Sci. 68, 651-659
161. Fausett, B. V., Gumerson, J. D. and Goldman, D. (2008) The proneural basic helix-loop-helix gene ascl1a is required for retina regeneration. J. Neurosci. 28, 1109-1117 (Pubitemid 351186339)
162. Ramachandran, R., Fausett, B. V. and Goldman, D. (2010) Ascl1a regulates Müller glia dedifferentiation and retinal regeneration through a Lin-28-dependent, let-7 microRNA signalling pathway. Nat. Cell Biol. 12, 1101-1107
163. Ramachandran, R., Zhao, X. F. and Goldman, D. (2011) Ascl1a/Dkk/β- catenin signaling pathway is necessary and glycogen synthase kinase-3β inhibition is sufficient for zebrafish retina regeneration. Proc. Natl. Acad. Sci. U.S.A. 108, 15858-15863
164. Thummel, R., Enright, J. M., Kassen, S. C., Montgomery, J. E., Bailey, T. J. and Hyde, D. R. (2010) Pax6a and Pax6b are required at different points in neuronal progenitor cell proliferation during zebrafish photoreceptor regeneration. Exp. Eye Res. 90, 572-582
165. Wan, J., Ramachandran, R. and Goldman, D. (2012) HB-EGF is necessary and sufficient for Müller glia dedifferentiation and retina regeneration. Dev. Cell 22, 334-347
166. Fischer, A. J. and Reh, T. A. (2001) Müller glia are a potential source of neural regeneration in the postnatal chicken retina. Nat. Neurosci. 4, 247-252 (Pubitemid 32194871)
167. Fischer, A. J. and Bongini, R. (2010) Turning Müller glia into neural progenitors in the retina. Mol. Neurobiol. 42, 199-209
168. Hayes, S., Nelson, B. R., Buckingham, B. and Reh, T. A. (2007) Notch signaling regulates regeneration in the avian retina. Dev. Biol. 312, 300-311 (Pubitemid 350186158)
169. Fischer, A. J., Scott, M. A., Ritchey, E. R. and Sherwood, P. (2009) Mitogen-activated protein kinase-signaling regulates the ability of Müller glia to proliferate and protect retinal neurons against excitotoxicity. Glia 57, 1538-1552
170. Fischer, A. J., Scott, M. A. and Tuten, W. (2009) Mitogen-activated protein kinase-signaling stimulates Müller glia to proliferate in acutely damaged chicken retina. Glia 57, 166-181
171. Fischer, A. J., McGuire, C. R., Dierks, B. D. and Reh, T. A. (2002) Insulin and fibroblast growth factor 2 activate a neurogenic program in
172. Ooto, S., Akagi, T., Kageyama, R., Akita, J., Mandai, M., Honda, Y. and Takahashi, M. (2004) Potential for neural regeneration after neurotoxic injury in the adult mammalian retina. Proc. Natl. Acad. Sci. U.S.A. 101, 13654-13659 (Pubitemid 39238458)
173. Osakada, F., Ooto, S., Akagi, T., Mandai, M., Akaike, A. and Takahashi, M. (2007) Wnt signaling promotes regeneration in the retina of adult mammals. J. Neurosci. 27, 4210-4219 (Pubitemid 46597155)
174. Das, A. V., Mallya, K. B., Zhao, X., Ahmad, F., Bhattacharya, S., Thoreson, W. B., Hegde, G. V. and Ahmad, I. (2006) Neural stem cell properties of Müller glia in the mammalian retina: regulation by Notch and Wnt signaling. Dev. Biol. 299, 283-302 (Pubitemid 44550105)
175. Bhatia, B., Singhal, S., Lawrence, J. M., Khaw, P. T. and Limb, G. A. (2009) Distribution of Müller stem cells within the neural retina: evidence for the existence of a ciliary margin-like zone in the adult human eye. Exp. Eye Res. 89, 373-382
176. Lawrence, J. M., Singhal, S., Bhatia, B., Keegan, D. J., Reh, T. A., Luthert, P. J., Khaw, P. T. and Limb, G. A. (2007) MIO-M1 cells and similar muller glial cell lines derived from adult human retina exhibit neural stem cell characteristics. Stem Cells 25, 2033-2043 (Pubitemid 47258181)
177. Wan, J., Zheng, H., Xiao, H. L., She, Z. J. and Zhou, G. M. (2007) Sonic hedgehog promotes stem-cell potential of Müller glia in the mammalian retina. Biochem. Biophys. Res. Commun. 363, 347-354 (Pubitemid 47484339)
178. Bhatia, B., Jayaram, H., Singhal, S., Jones, M. F. and Limb, G. A. (2011) Differences between the neurogenic and proliferative abilities of Müller glia with stem cell characteristics and the ciliary epithelium from the adult human eye. Exp. Eye Res. 93, 852-861
179. Tsonis, P. A. and Makarev, E. (2008) On dorsal/ventral-specific genes in the iris during lens regeneration. Cell. Mol. Life Sci. 65, 41-44
180. Spence, J., Gutierrez, C and Del Rio-Tsonis, K. (2008) Retina regeneration in the embryonic chick. In Strategies for Retinal Tissue Repair and Regeneration in Vertebrates: From Fish to Human (Chiba, C., ed.), pp. 97-112, Research Signpost, Trivandrum
181. Gehring, W. J. (2011) Chance and necessity in eye evolution. Genome Biol. Evol. 3, 1053-1066
182. Graw, J. (1996) Genetic aspects of embryonic eye development in vertebrates. Dev. Genet. 18, 181-197
183. Halder, G., Callaerts, P. and Gehring, W. J. (1995) Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science 267, 1788-1792
184. Fischer, A. J. and Reh, T. A. (2001) Transdifferentiation of pigmented epithelial cells: a source of retinal stem cells? Dev. Neurosci. 23, 268-276 (Pubitemid 34045221)
185. Cvekl, A. and Mitton, K. P. (2010) Epigenetic regulatory mechanisms in vertebrate eye development and disease. Heredity 105, 135-151
186. Sanchez Alvarado, A. and Tsonis, P. A. (2006) Bridging the regeneration gap: genetic insights from diverse animal models. Nat. Rev. Genet. 7, 873-884
187. Tsonis, P. A. and Del Rio-Tsonis, K. (2004) Lens and retina regeneration: transdifferentiation, stem cells and clinical applications. Exp. Eye Res. 78, 161-172 (Pubitemid 38077224)