Gene Regulation During Axon and Tissue Regeneration in the Retina of Zebrafish

Model Organisms in Spinal Cord Regeneration

Volumn , Issue , 2007, Pages 373-394

  Senut, Marie Claude ^a   Fausett, Blake ^a   Veldman, Matthew ^a   Goldman, Daniel ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Axon and tissue regenation in the retina of zebrafish; Gene regulation; Optic nerve lesion; Optic nerve regeneration; Retina injury; Zebrafish retina

Indexed keywords

EID: 52649147930     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9783527610365.ch13     Document Type: Chapter

References (87)

1. Asch, W.S., Leake, D., Canger, A.K., Passini M.A., Argenton, F., Schechter, N., Cloning of zebrafish neurofilament cDNAs for plasticin and gefiltin: increased mRNA expression in ganglion cells after optic nerve injury. J. Neurochem. 1998, 71, 20-32.
2. Avanesov, A., Dahm, R., Sewell, W.F., Malicki, J.J., and the Tuebingen 2000 Screening Consortium, Mutations that affect the survival of selected amacrine cell subpopulations define a new class of genetic defects in the vertebrate retina. Dev. Biol. 2005, 285, 138-155.
3. Ballestero, R.P., Dybowski, J.A., Levy, G., Agranoff, B.W., Uhler, M.D., Cloning and characterization of zRICH, a 2', 3'-cyclic-nucleotide 3 '-phosphodiesterase induced during zebrafish optic nerve regeneration. J. Neurochem. 1999, 72, 1362-1371.
4. Becker, C.G., Becker, T., Repellent guidance of regenerating optic axons by chondroitin sulfate glycosaminoglycans in zebrafish. J. Neurosci. 2002, 22, 842-853.
5. Becker, C.G., Lieberoth, B.C., Morellini, F., Feldner, J., Becker, T., Schachner, M., L1.1 is involved in spinal cord regeneration in adult zebrafish. J. Neurosci. 2004, 24, 7837-7842.
6. Becker, C.G., Meyer, R.L., Becker, T., Gradients of ephrin-A2 and ephrin-A5b mRNA during retinotopic regeneration of the optic projection in adult zebrafish. J. Comp. Neurol. 2000, 427, 469-483.
7. Becker, C.G., Schweitzer, J., Feldner, J., Schachner, M., Becker, T., Tenascin-R as a repellent guidance molecule for newly growing and regenerating optic axons in adult zebrafish. Mol. Cell. Neurosci. 2004, 26, 376-389.
8. Bernhardt, R.R., Tongiorgi, E., Anzini, P., Schachner, M., Increased expression of specific recognition molecules by retinal ganglion cells and by the optic pathway glia accompanies the successful regeneration of retinal axons in adult zebrafish. J. Comp. Neurol. 1996, 376, 253-264.
9. Bernhardt, R.R., Cellular and molecular bases of axonal regeneration in the fish central nervous system. Exp. Neurol. 1999, 157, 223-240.
10. Bormann, P., Roth, L.W., Andel, D., Ackermann, M., Reinhard, E., Zfnlrr, a novel leucine-rich repeat protein is preferentially expressed during regeneration in zebrafish. Mol. Cell. Neurosci. 1999, 13, 167-179.
11. Bormann, P., Zumsteg, V.M., Roth, L.W., Reinhard, E., Target contact regulates GAP-43 and alpha-tubulin mRNA levels in regenerating retinal ganglion cells. J. Neurosci. Res. 1998, 52, 405-419.
12. Braisted, J.E., Essman, T.F., Raymond, P.A., Selective regeneration of photoreceptors in goldfish retina. Development 1994, 120, 2409-2419.
13. Braisted, J.E., Raymond, P.A., Regeneration of dopaminergic neurons in goldfish retina. Development 1992, 114, 913-919.
14. Cameron, D.A., Carney, L.H., Cellular patterns in the inner retina of adult zebrafish: quantitative analyses and a computational model of their formation. J. Comp. Neurol. 2004, 471, 11-25.
15. Cameron, D.A., Gentile, K.L., Middleton, F.A., Yurco, P., Gene expression profiles of intact and regenerating zebrafish retina. Mol. Vision 2005, 11, 775-791.
16. Cameron, D.A., Cellular proliferation and neurogenesis in the injured retina of adult zebrafish. Vis. Neurosci. 2000, 17, 789-797.
17. Cuiverwell, J., Karistrom, R.O., Making the connection: retinal axon guidance in the zebrafish. Semin. Cell Dev. Biol. 2002, 13, 497-506.
18. Detrich III, H.W., Westerfield, M., Zon, L.I., The zebrafish, genetics and genomics. Academic Press, 1999.
19. Dlekmann, H., Klinger, M., Oertle, T., Heinz, D., Pogoda, H.-M., Schwab, M.E., Stuermer, C.A.O., Analysis of the reticulon gene family demonstrates the absence of the neurite growth inhibitor Nogo-A in fish. Mol. Biol. Evol. 2005, 22, 1635-1648.
20. Doerre, G., Malicki, J., Genetic analysis of photoreceptor cell development in the zebrafish retina. Mech. Dev. 2002, 110, 125-138.
21. Easter, S.S. Jr., Nicoia, G.N., The development of vision in the zebrafish. Dev. Biol. 1996, 180, 646-663.
22. Ekker, S.C., Morphants: a new systematic vertebrate functional genomics approach. Yeast 2000, 17, 302-306.
23. Fausett, B., Goldman, D., A role for α 1 tubulin-expressing Muller glia in regeneration of the injured zebrafish retina. J. Neurosci. 2006, 26, 6303-6313.
24. Fischer, A.J., Reh, T.A., Muller glia are a potential source of neural regeneration in the postnatal chick retina. Nat. Neurosci. 2001, 4, 247-252.
25. Garcia-Crespo, D., Vecino, E., Differential expression of calretinin in the developing and regenerating zebrafish visual system. Histol. Histopathol. 2004, 19, 1193-1199.
26. Giraidez, A.J., Cinalli, R.M., Glasner, M.E., Enright, A.J., Thomson, J.M., Basker-Ville, S., Hammond, S.M., Bartel, D.P., Schier, A.F., MicroRNAs regulate brain morphogenesis in zebrafish. Science 2005, 308, 833-838.
27. Goldman, D., Ding, J., Different regulatory elements are necessary for alpha1 tubulin induction during CNS development and regeneration. NeuroReport 2000, 11, 3859-3863.
28. Goldman, D., Hankin, M., Li, Z., Dai, X., Ding, J., Transgenic zebrafish for studying nervous system development and regeneration. Transgenic Res. 2001, 10, 21-33.
29. Gross, J.M., Perkins, B.D., Amsterdam, A., Egana, A., Dariand, T., Matsui, J.I., Sciascia, S., Hopkins, N., Dowling, J.E., Identification of zebrafish insertional mutants with defects in visual system development and function. Genetics 2005, 170, 245-261.
30. Halloran, M.C., Sato-Maeda, M., Warren, J.T., Su, F., Lele, Z., Krone, P.H., Kuwada, J.Y., Shoji, W., Laser-induced expression in specific cells in transgenic fish. Development 2000, 127, 1953-1960.
31. Herdegen, T., Bastmeyer, M., Bahr, M., Stuermer, C., Bravo, R., Zimmermann, M., Fibroblast growth factor-inducible-14 is induced in axotomized neurons and promotes neurite outgrowth. J. Neurobiol. 1993, 24, 528-543.
32. Hieber, V., Dai, X., Foreman, M., Goidman, D., Induction of alpha1-tubulin gene expression during development and regeneration of the fish central nervous system. J. Neurobiol. 1998, 37, 429-440.
33. Hitchcock, P.F., Macdonald, R.E., Vanderyt, J.T., Wiison, S.W., Antibodies against Pax6 immunostain amacrine and ganglion cells and neuronal progenitors, but not rod precursors, in the normal and regenerating retina of the goldfish. J. Neurobiol. 1996, 29, 399-413.
34. Hitchcock, P., Ochocinska, M., Sleh, A., Otteson, D., Persistent and injury-induced neurogenesis in the vertebrate retina. Prog. Retinal Eye Res. 2004, 23, 183-194.
35. Horner, P.J., Gage, F.H., Regenerating the damaged central nervous system. Nature 2000, 407, 963-970.
36. Huang, C.-J., Jou, T.-S., Ho, Y.-L., Lee, W.-H., Jeng, Y.-T., Hsieh, F.-J., Tsai, H.-J., Conditional expression of a myocardium-specific transgene in zebrafish transgenic lines. Dev. Dyn. 2005, 233, 1294-1303.
37. Huber, A.B., Schwab, M.E., Nogo-A a potent inhibitor of neurite outgrowth and regeneration. Biol. Chem. 2000, 381, 407-419.
38. Hutson, L.D., Chien, C.-B., Pathfinding and error correction by retinal axons: the role of astray/robo2. Neuron 2002, 33, 205-217.
39. Kawakami, K., Transposon tools and methods in zebrafish. Dev. Dyn. 2005, 234, 244-254.
40. Kay, J.N., Finger-Baier, K.C., Roeser, T., Staub, W., Baier, H., Retinal ganglion cell genesis require lakritz, a zebrafish atonal homolog. Neuron 2001, 30, 625-736.
41. Kiinger, M., Taylor, J.S., Oertle, T., Schwab, M.E., Stuermer, C.A.O., Diekmann, H., Identification of Nogo-66 receptor (NgR) and homologous genes in fish. Mol. Biol. Evol. 2004, 21, 76-85.
42. Koopman, P., Schepers, G., Brenner, S., Venkatesh, B., Origin and diversity of the Sox transcription factor gene family: genome-wide analysis in Fugu rubripes. Gene 2004, 328, 177-186.
43. Lang, D.M., Warren Jr, J.T., Klisa, C., Stuermer, C.A., Topographic restriction of TAG-1 expression in the developing retinotectal pathway and target dependent reexpression during axon regeneration. Mol. Cell. Neurosci. 2001, 17, 398-414.
44. Langenau, D.M., Feng, H., Berghmans, S., Kanki, J.P., Kutok, J.L., Look, A.T., Cre/lox-regulated transgenic zebrafish model with conditional myc-induced T cell acute lymphoblastic leukemia. Proc. Natl. Acad. Sci. USA 2005, 102, 6068-6073.
45. Levine, E.M., Hitchcock, P.F., Glasgow, E., Schechter, N., Restricted expression of a new paired-class homeobox gene in normal and regenerating adult goldfish retina. J. Comp. Neurol. 1994, 348, 596-606.
46. Li, Z., Joseph, N.M., Easter Jr, S.S., The morphogenesis of the zebrafish eye, including a fate map of the optic vesicle. Dev. Dyn. 2000, 218, 175-188.
47. Lillo, C., Velasco, A., Mimeno, D., Cid, E., Aijon, J., Lara, J.M., Non-neuronal cells involved in the degeneration and regeneration of the fish retina. J. Neurocytol. 2001, 30, 475-491.
48. Liu, Q., Londraville, R.L., Azodi, E., Babb, S.G., Chiappini-Williamson, C., Marrs, J.A., Raymond, P.A., Up-regulation of cadherin-2 and cadherin-4 in regenerating visual structures of adult zebrafish. Exp. Neurol. 2002, 177, 396-406.
49. Liu, Z.W., Matsukawa, T., Arai, K., Devadas, M., Nakashima, H., Tanaka, M., Mawa-Tari, K., Kato, S., Na, K-ATPase α3 sub-unit in the goldfish retina during optic nerve regeneration. J. Neurochem. 2002, 80, 763-770.
50. Mager, J., Bartoiomei, M.S., Strategies for dissecting epigenetic mechanisms in the mouse. Nat. Genet. 2005, 37, 1194-1200.
51. Maiicki, J.J., Development of the retina. Methods Cell Biol. 1999, 273-299.
52. Malicki, J., Harnessing the power of forward genetics-analysis of neuronal diversity and patterning in the zebrafish retina. Trends Neurosci. 2000, 23, 531-541.
53. Malicki, J., Jo, H., Wei, X., Hsiung, M., Pujic, Z., Analysis of gene function in the zebrafish retina. Methods 2002a, 28, 427-438.
54. Malicki, J.J., Pujic, Z., Thisse, C., Thisse, B., Wei, X., Forward and reverse genetic approaches to the analysis of eye development in zebrafish. Vision Res. 2002b, 42, 527-533.
55. Matsukawa, T., Sugitani, K., Mawatari, K., Koriyama, Y., Liu, Z., Tanaka, M., Kato, S., Role of pupurin as a retinol-binding protein in goldfish retina during the early stage of optic nerve regeneration: its priming action on neurite outgrowth. J. Neurosci. 2004, 24, 8346-8353.
56. Mcdowell, A.L., Dixon, L.J., Houchins, J.D., Bilotta, J., Visual processing of the zebrafish optic tectum before and after optic nerve damage. Vis. Neurosci. 2004, 21, 97-106.
57. Mullins, M.C., Hammerschmidt, M., Haffter, P., Nusslein-Volhard, C., Large-scale mutagenesis in the zebrafish: in search of genes controlling development in a vertebrate. Curr. Biol. 1994, 4, 189-202.
58. Neuhauss, S.C.F., Behavioral genetic approaches to visual system development and function in zebrafish. J. Neurobiol. 2003, 54, 148-160.
59. Nieisen, A.L., Jorgensen, A.L., Structural and functional characterization of the zebrafish gene for glial fibrillary protein, GFAP. Gene 2003, 310, 123-132.
60. Ooto, S., Akagi, T., Kageyama, R., Akita, J., Mandai, M., Honda, Y., Takahashi, M., Potential for neural regeneration after neurotoxic injury in the adult mammalian retina. Proc. Natl. Acad. Sci. USA 2004, 101, 13654-13659.
61. Otteson, D.C., Cirenza, P.F., Hitchcock, P.F., Persistent neurogenesis in the teleost retina: Evidence for regulation by the growth-hormone/insulin-like growth factor-I axis. Mech. Dev. 2002, 117, 137-149.
62. Otteson, D.C., Hitchcock, P.F., Stem cells in the teleost retina: persistent neurogenesis and injury-induced regeneration. Vision Res. 2003, 43, 927-936.
63. Peterson, R.E., Fadool, J.M., Mcclintock, J., Linser, P.J., Müller cell differentiation in the zebrafish neural retina: evidence of distinct early and late stages in cell maturation. J. Comp. Neurol. 2001, 429, 530-540.
64. Petrausch, B., Tablblazar, R., Roser, T., Jing, Y., Goidman, D., Stuermer, C.A.O., Irwin, N., Benowitz, L.I., A purine-sensitive pathway regulates multiple genes involved in axon regeneration in goldfish retinal ganglion cells. J. Neurosci. 2000, 20, 8031-8041.
65. Pujic, Z., Malicki, J., Retinal pattern and the genetic basis of its formation in zebrafish. Semin. Cell Dev. Biol. 2004, 15, 105-114.
66. Roth, L.W.A., Bormann, P., Wlederkehr, C., Reinhard, E., b-thymosin, a modulator of the actin cytoskeleton is increased in regenerating retinal ganglion cell. Eur. J. Neurosci. 1999, 11, 3488-3498.
67. Scheer, N., Groth, A., Hans, S., Campos-Ortega, J.A., An instructive function for Notch in promoting gliogenesis in the zebrafish retina. Development 2001, 128, 1099-1107.
68. Schmidt, J.T., Buzzard, M., Borress, R., Dhillon, S., MK801 increases retinotectal arbor size in developing zebrafish without affecting kinetics of branch elimination and addition. J. Neurobiol. 2000, 42, 303314.
69. Schmitt, E.A., Dowling, J.E., Early retinal development in the zebrafish, Danio rerio: light and electron microscopic analyses. J. Comp. Neurol. 1999, 404, 515-536.
70. Schweitzer, J., Becker, T., Becker, C.G., Schachner, M., Expression of protein zero is increased in lesioned axon pathways in the central nervous system of adult zebra-fish. Glia 2003, 41, 301-317.
71. Senut, M.-C., Guiati-Leekha, A., Goldman, D., An element in the α 1-tubulin promoter is necessary for retinal expression during optic nerve regeneration but not after eye injury in the adult zebrafish. J. Neurosci. 2004, 24, 7663-7673.
72. Sperry, R.W., Patterning of central synapses in regeneration of the optic nerve in teleosts. Physiol. Zool. 1948, 21, 351-361.
73. Stuermer, C.A., Plattner, H., The 'lipid raft' microdomain proteins reggie-1 and reggie-2 (flotillins) are scaffolds for protein interaction and signaling. Biochem. Soc. Symp. 2005, 72, 109-118.
74. Stuermer, C.A., Rohrer, B., Munz, H., Development of the retinotectal projection in zebrafish embryos under TTX-induced neural-impulse blockade. J. Neurosci. 1990, 10, 3615-3626.
75. Stuermer, C.A.O., Retinotopic organization of the developing retino-tectal projection in the zebrafish embryo. J. Neurosci. 1988, 8, 4513-4530.
76. Sullivan, S.A., Barthel, L.K., Largent, B.L., Raymond, P.A., A goldfish notch-3 homologue is expressed in neurogenic regions of embryonic, adult, and regenerating brain and retina. Dev. Genet. 1997, 20, 208-223.
77. Tanabe, K., Bonilla, I., Wlnkles, J.A., Strittmatter, S.M., J. Neurosci. 2003, 23, 9675-9686.
78. Udvadia, A.J., Koster, R.W., Skene, J.H., GAP-43 promoter elements in transgenic zebrafish reveal a difference in signals for axon growth during CNS development and regeneration. Development 2001, 128, 1175-1182.
79. Verma, P., Chierzi, S., Codd, A.M., Campbell, D.S., Meyer, R.L., Holt, C.E., Fawcett, J.W., Axonal protein synthesis and degradation are necessary for efficient growth cone regeneration. J. Neurosci. 2005, 25, 331-342.
80. Vihtelic, T.S., Hyde, D.R., Light-induced rod and cone cell death and regeneration in the adult albino zebrafish (Danio rerio) retina. J. Neurobiol. 2000, 44, 289-307.
81. Vihtelic, T.S., Soverly, J.E., Kassen, S.C., Hyde, D.R., Retinal regional differences in photoreceptor cell death and regeneration in light-lesioned albino zebrafish. Exp. Eye Res. 2005, 82, 558-575.
82. Wehman, A.M., Staub, W., Meyers, J.R., Raymond, P.A., Baier, H., Genetic dissection of the zebrafish retinal stem-cell compartment. Dev. Biol. 2005, 281, 53-65.
83. Wienholds, E., Kloosterman, W.P., Miska, E., Alvarez-Saavedra, E., Berezikov, E., De Bruijn, E., Horvitz, H.R., Kauppinen, S., Piasterk, R.H., MicroRNA expression in zebrafish embryonic development. Science 2005, 309, 310-311.
84. Wu, D.M., Schneiderman, T., Burgett, J., Gokhale, P., Barthel, L., Raymond, P.A., Cones regenerate from retinal stem cells sequestered in the inner nuclear layer of adult goldfish retina. Invest. Ophthalmol. Vis. Sci. 2001, 42, 2115-2124.
85. Xiao, T., Roeser, T., Staub, W., Baier, H., A GFP-based genetic screen reveals mutations that disrupt the architecture of the zebrafish retino-tectal projection. Development 2005, 132, 2955-2967.
86. Yiu, G., He, Z., Signaling mechanisms of the myelin inhibitors of axon regeneration. Curr. Opin. Neurobiol. 2003, 13, 545-551.
87. Yurco, P., Cameron, D.A., Responses of Muller glia to retinal injury in adult zebra-fish. Vision Res. 2005, 45, 991-1002.