Regeneration of Cone Photoreceptors when Cell Ablation Is Primarily Restricted to a Particular Cone Subtype

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Fraser, Brittany ^a   DuVal, Michèle G ^a   Wang, Hao ^a   Allison, W Ted ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

METRONIDAZOLE; NITROREDUCTASE; OPSIN; PROTEIN VP16; TRANSCRIPTION FACTOR GAL4;

ABLATION THERAPY; AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BYSTANDER EFFECT; CELL DEATH; CELL DIFFERENTIATION; CELL FATE; CELL POPULATION; CELL PROLIFERATION; CELL REGENERATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RETINA CONE; RETINA DEVELOPMENT; RETINA ROD; TISSUE REGENERATION; TRANSGENIC ANIMAL; WILD TYPE; ZEBRA FISH;

ABLATION TECHNIQUES; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BROMODEOXYURIDINE; CRYOULTRAMICROTOMY; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; IN SITU NICK-END LABELING; METRONIDAZOLE; MODELS, ANIMAL; NITROREDUCTASES; REGENERATION; RETINAL CONE PHOTORECEPTOR CELLS; STATISTICS, NONPARAMETRIC; STEM CELLS; ZEBRAFISH;

EID: 84873813858     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0055410     Document Type: Article

References (83)

1. Cameron DA, Easter SS, (1995) Cone photoreceptor regeneration in adult fish retina: phenotypic determination and mosaic pattern formation. J Neurosci 15: 2255-2271.
2. Otteson DC, Hitchcock PF, (2003) Stem cells in the teleost retina: persistent neurogenesis and injury-induced regeneration. Vision Res 43: 927-936.
3. Raymond PA, Reifler MJ, Rivlin PK, (1988) Regeneration of goldfish retina: rod precursors are a likely source of regenerated cells. J Neurobiol 19: 431-463.
4. Hitchcock PF, Raymond PA, (2004) The zebrafish retina as a model for developmental and regeneration biology. Zebrafish 1: 257-271.
5. Easter SS, Hitchcock PF, (2000) Stem cells and regeneration in the retina: What fish have taught us about neurogenesis. Neuroscientist 6: 454-464.
6. Vihtelic TS, Hyde DR, (2000) Light-induced rod and cone cell death and regeneration in the adult albino zebrafish (Danio rerio) retina. J Neurobiol 44: 289-307.
7. Allison WT, Hallows TE, Johnson T, Hawryshyn CW, Allen DM, (2006) Photic history modifies susceptibility to retinal damage in albino trout. Vis Neurosci 23: 25-34.
8. Allison WT, Dann SG, Veldhoen KM, Hawryshyn CW, (2006) Degeneration and regeneration of ultraviolet cone photoreceptors during development in rainbow trout. J Comp Neurol 499: 702-715.
9. Browman HI, Hawryshyn CW, (1992) Thyroxine induces a precocial loss of ultraviolet photosensitivity in rainbow trout (Oncorhynchus mykiss, Teleostei). Vision Res 32: 2303-2312.
10. Allison WT, Dann SG, Helvik JV, Bradley C, Moyer HD, et al. (2003) Ontogeny of ultraviolet-sensitive cones in the retina of rainbow trout (Oncorhynchus mykiss). Journal of Comparative Neurology 461: 294-306.
11. Beaudet L, Browman HI, Hawryshyn CW, (1993) Optic nerve response and retinal structure in rainbow trout of different sizes. Vision Res 33: 1739-1746.
12. Novales Flamarique I, Hawryshyn C, (1996) Retinal development and visual sensitivity of young Pacific sockeye salmon (Oncorhynchus nerka). J Exp Biol 199: 869-882.
13. Fleisch VC, Fraser B, Allison WT, (2011) Investigating regeneration and functional integration of CNS neurons: Lessons from zebrafish genetics and other fish species. Biochimica et Biophysica Acta-Molecular Basis of Disease 1812: 364-380.
14. Cayouette M, Poggi L, Harris WA, (2006) Lineage in the vertebrate retina. Trends Neurosci 29: 563-570.
15. Cepko CL, (1999) The roles of intrinsic and extrinsic cues and bHLH genes in the determination of retinal cell fates. Curr Opin Neurobiol 9: 37-46.
16. Turner DL, Snyder EY, Cepko CL, (1990) Lineage-independent determination of cell type in the embryonic mouse retina. Neuron 4: 833-845.
17. Reh TA, (1992) Cellular interactions determine neuronal phenotypes in rodent retinal cultures. J Neurobiol 23: 1067-1083.
18. Reh TA, Cagan RL, (1994) Intrinsic and extrinsic signals in the developing vertebrate and fly eyes: viewing vertebrate and invertebrate eyes in the same light. Perspect Dev Neurobiol 2: 183-190.
19. West EL, Gonzalez-Cordero A, Hippert C, Osakada F, Martinez-Barbera JP, et al. (2012) Defining the Integration Capacity of ES Cell-Derived Photoreceptor Precursors. Stem Cells.
20. Lakowski J, Baron M, Bainbridge J, Barber AC, Pearson RA, et al. (2010) Cone and rod photoreceptor transplantation in models of the childhood retinopathy Leber congenital amaurosis using flow-sorted Crx-positive donor cells. Hum Mol Genet 19: 4545-4559.
21. Inoue T, Coles BL, Dorval K, Bremner R, Bessho Y, et al. (2010) Maximizing functional photoreceptor differentiation from adult human retinal stem cells. Stem Cells 28: 489-500.
22. Jomary C, Jones SE, Lotery AJ, (2010) Generation of light-sensitive photoreceptor phenotypes by genetic modification of human adult ocular stem cells with Crx. Invest Ophthalmol Vis Sci 51: 1181-1189.
23. Jomary C, Jones SE, (2008) Induction of functional photoreceptor phenotype by exogenous Crx expression in mouse retinal stem cells. Invest Ophthalmol Vis Sci 49: 429-437.
24. MacLaren RE, Pearson RA, MacNeil A, Douglas RH, Salt TE, et al. (2006) Retinal repair by transplantation of photoreceptor precursors. Nature 444: 203-207.
25. Pearson RA, Barber AC, Rizzi M, Hippert C, Xue T, et al. (2012) Restoration of vision after transplantation of photoreceptors. Nature 485: 99-103.
26. Lakowski J, Han YT, Pearson RA, Gonzalez-Cordero A, West EL, et al. (2011) Effective transplantation of photoreceptor precursor cells selected via cell surface antigen expression. Stem Cells 29: 1391-1404.
27. Gust J, Reh TA, (2011) Adult donor rod photoreceptors integrate into the mature mouse retina. Invest Ophthalmol Vis Sci 52: 5266-5272.
28. Engstom K, (1960) Cone types and cone arrangements in the retina of some cyprinids. Acta Zoologica (Stockh) 41: 277-295.
29. Raymond PA, Barthel LK, (2004) A moving wave patterns the cone photoreceptor mosaic array in the zebrafish retina. Int J Dev Biol 48: 935-945.
30. Raymond PA, Barthel LK, Rounsifer ME, Sullivan SA, Knight JK, (1993) Expression of rod and cone visual pigments in goldfish and zebrafish: a rhodopsin-like gene is expressed in cones. Neuron 10: 1161-1174.
31. Allison WT, Barthel LK, Skebo KM, Takechi M, Kawamura S, et al. (2010) Ontogeny of Cone Photoreceptor Mosaics in Zebrafish. Journal of Comparative Neurology 518: 4182-4195.
32. Eglen SJ, Wong JCT, (2008) Spatial constraints underlying the retinal mosaics of two types of horizontal cells in cat and macaque. Visual Neuroscience 25: 209-214.
33. Togashi H, Kominami K, Waseda M, Komura H, Miyoshi J, et al. (2011) Nectins establish a checkerboard-like cellular pattern in the auditory epithelium. Science 333: 1144-1147.
34. Rister J, Desplan C, (2011) The retinal mosaics of opsin expression in invertebrates and vertebrates. Dev Neurobiol 71: 1212-1226.
35. Hartman BH, Reh TA, Bermingham-McDonogh O, (2010) Notch signaling specifies prosensory domains via lateral induction in the developing mammalian inner ear. Proc Natl Acad Sci U S A 107: 15792-15797.
36. Cameron DA, Carney LH, (2000) Cell mosaic patterns in the native and regenerated inner retina of zebrafish: implications for retinal assembly. J Comp Neurol 416: 356-367.
37. Stenkamp DL, Cameron DA, (2002) Cellular pattern formation in the retina: retinal regeneration as a model system. Molecular Vision 8: 280-293.
38. Johns PR, Fernald RD, (1981) Genesis of rods in teleost fish retina. Nature 293: 141-142.
39. Perron M, Harris WA, (2000) Retinal stem cells in vertebrates. Bioessays 22: 685-688.
40. Lyall AH, (1957) The growth of the trout retina. Quar J Micro Sci 98: 101-110.
41. Lyall AH, (1957) Cone arrangements in teleost retinae. Quar J Micro Sci 98: 189-201.
42. Stenkamp DL, Barthel LK, Raymond PA, (1997) Spatiotemporal coordination of rod and cone photoreceptor differentiation in goldfish retina. J Comp Neurol 382: 272-284.
43. Allison WT (2004) Rainbow trout as a model of retinal photoreceptor death and regeneration; Ph. D. thesis. Victoria, BC, Canada: University of Victoria.205 p.
44. Veldhoen K, Allison WT, Veldhoen N, Anholt BR, Helbing CC, et al. (2006) Spatio-temporal characterization of retinal opsin gene expression during thyroid hormone-induced and natural development of rainbow trout. Vis Neurosci 23: 169-179.
45. Davison JM, Akitake CM, Goll MG, Rhee JM, Gosse N, et al. (2007) Transactivation from Gal4-VP16 transgenic insertions for tissue-specific cell labeling and ablation in zebrafish. Developmental Biology 304: 811-824.
46. Goll MG, Anderson R, Stainier DYR, Spradling AC, Halpern ME, (2009) Transcriptional Silencing and Reactivation in Transgenic Zebrafish. Genetics 182: 747-755.
47. Li FY, Papworth M, Minczuk M, Rohde C, Zhang YY, et al. (2007) Chimeric DNA methyltransferases target DNA methylation to specific DNA sequences and repress expression of target genes. Nucleic Acids Research 35: 100-112.
48. Akitake CM, Macurak M, Halpern ME, Goll MG, (2011) Transgenerational analysis of transcriptional silencing in zebrafish. Dev Biol 352: 191-201.
49. Takechi M, Hamaoka T, Kawamura S, (2003) Fluorescence visualization of ultraviolet-sensitive cone photoreceptor development in living zebrafish. FEBS Lett 553: 90-94.
50. Montgomery JE, Parsons MJ, Hyde DR, (2010) A Novel Model of Retinal Ablation Demonstrates That the Extent of Rod Cell Death Regulates the Origin of the Regenerated Zebrafish Rod Photoreceptors. Journal of Comparative Neurology 518: 800-814.
51. Curado S, Stainier DYR, Anderson RM, (2008) Nitroreductase-mediated cell/tissue ablation in zebrafish: a spatially and temporally controlled ablation method with applications in developmental and regeneration studies. Nature Protocols 3: 948-954.
52. Edwards DI, (1993) Nitroimidazole drugs- action and resistance mechanisms.1. mechanisms of action. Journal of Antimicrobial Chemotherapy 31: 201-210.
53. Pisharath H, Rhee JM, Swanson MA, Leach SD, Parsons MJ, (2007) Targeted ablation of beta cells in the embryonic zebrafish pancreas using E-coli nitroreductase. Mechanisms of Development 124: 218-229.
54. Zhao XF, Ellingsen S, Fjose A, (2009) Labelling and targeted ablation of specific bipolar cell types in the zebrafish retina. BMC Neurosci 10: 107.
55. Ariga J, Walker SL, Mumm JS (2010) Multicolor time-lapse imaging of transgenic zebrafish: visualizing retinal stem cells activated by targeted neuronal cell ablation. J Vis Exp: e2093.
56. Kee N, Sivalingam S, Boonstra R, Wojtowicz JM, (2002) The utility of Ki-67 and BrdU as proliferative markers of adult neurogenesis. Journal of Neuroscience Methods 115: 97-105.
57. Thummel R, Kassen SC, Enright JM, Nelson CM, Montgomery JE, et al. (2008) Characterization of Muller glia and neuronal progenitors during adult zebrafish retinal regeneration. Experimental Eye Research 87: 433-444.
58. Bernardos RL, Barthel LK, Meyers JR, Raymond PA, (2007) Late-stage neuronal progenitors in the retina are radial Muller glia that function as retinal stem cells. Journal of Neuroscience 27: 7028-7040.
59. Bernardos RL, Barthel LK, Raymond PA, (2005) Localized retinal regeneration following thermal lesions in adult zebrafish. Investigative Ophthalmology & Visual Science 46: 5327.
60. Fernald RD (1990) Teleost vision: seeing while growing. J Exp Zool Suppl 5: 167-180.
61. Raymond PA (1991) Retinal regeneration in teleost fish. Ciba Found Symp. 160: 171-186; discussion 186-191.
62. Raymond PA, Hitchcock PF, (2004) The teleost retina as a model for developmental and regeneration biology. Zebrafish 1: 257-271.
63. Fausett BV, Goldman D, (2006) A role for alpha1 tubulin-expressing Muller glia in regeneration of the injured zebrafish retina. J Neurosci 26: 6303-6313.
64. Ramachandran R, Reifler A, Parent JM, Goldman D, (2010) Conditional gene expression and lineage tracing of tuba1a expressing cells during zebrafish development and retina regeneration. J Comp Neurol 518: 4196-4212.
65. Beaudet L, Hawryshyn CW (1999) Ecological aspects of vertebrate visual ontogeny. In: Archer SN, Djamgoz MBA, Loew ER, Partridge JC, Vallerga S, editors. Adaptive mechanisms in the ecology of vision. Dordrecht,The Netherlands: Kluwer Academic Publishers. 413-437.
66. DuVal MG, Cheung H, Lehmann OJ, Allison WT (2012) Longitudinal fluorescent observation of retinal degeneration and regeneration in zebrafish using fundus lens imaging. (Accepted pending minor revison at Molecular Vision).
67. Easter SS, (1992) Retinal growth in foveated teleosts: nasotemporal asymmetry keeps the fovea in temporal retina. J Neurosci 12: 2381-2392.
68. Allison WT, Haimberger TJ, Hawryshyn CW, Temple SE, (2004) Visual pigment composition in zebrafish: Evidence for a rhodopsin-porphyropsin interchange system. Vis Neurosci 21: 945-952.
69. Allison WT, Veldhoen KM, Hawryshyn CW, (2006) Proteomic analysis of opsins and thyroid hormone-induced retinal development using isotope-coded affinity tags (ICAT) and mass spectrometry. Molecular Vision 12: 655-672.
70. Temple SE, Veldhoen KM, Phelan JT, Veldhoen NJ, Hawryshyn CW, (2008) Ontogenetic changes in photoreceptor opsin gene expression in coho salmon (Oncorhynchus kisutch, Walbaum). J Exp Biol 211: 3879-3888.
71. Alvarez-Delfin K, Morris AC, Snelson CD, Gamse JT, Gupta T, et al. (2009) Tbx2b is required for ultraviolet photoreceptor cell specification during zebrafish retinal development. Proc Natl Acad Sci U S A 106: 2023-2028.
72. Bernardos RL, Lentz SI, Wolfe MS, Raymond PA (2004) Notch-Delta signaling is required for spatial patterning and Müller glia differentiation in the zebrafish retina. Journal of Comparative Neurology. In press.
73. Eglen SJ, Willshaw DJ, (2002) Influence of cell fate mechanisms upon retinal mosaic formation: a modelling study. Development 129: 5399-5408.
74. Eglen SJ, Galli-Reta L (2006) Retinal Mosaics. In: Sernagor E, Eglen SJ, Harris WA, Wong R, editors. Retinal Development.Cambridge: Cambridge University Press. 193-207.
75. Eglen SJ, van Ooyen A, Willshaw DJ, (2000) Lateral cell movement driven by dendritic interactions is sufficient to form retinal mosaics. Network 11: 103-118.
76. Mochizuki A, (2002) Pattern formation of the cone mosaic in the zebrafish retina: A cell rearrangement model. Journal of Theoretical Biology 215: 345-361.
77. Tohya S, Mochizuki A, Iwasa Y, (1999) Formation of cone mosaic of zebrafish retina. Journal of Theoretical Biology 200: 231-244.
78. Tohya S, Mochizuki A, Iwasa Y, (2003) Difference in the retinal cone mosaic pattern between zebrafish and medaka: Cell-rearrangement model. Journal of Theoretical Biology 221: 289-300.
79. Bhatia B, Jayaram H, Singhal S, Jones MF, Limb GA, (2011) Differences between the neurogenic and proliferative abilities of Muller glia with stem cell characteristics and the ciliary epithelium from the adult human eye. Exp Eye Res 93: 852-861.
80. Giannelli SG, Demontis GC, Pertile G, Rama P, Broccoli V, (2011) Adult human Muller glia cells are a highly efficient source of rod photoreceptors. Stem Cells 29: 344-356.
81. Lamba DA, Karl MO, Reh TA, (2009) Strategies for retinal repair: cell replacement and regeneration. Prog Brain Res 175: 23-31.
82. Westerfield M (2000) The zebrafish book. A guide for the laboratory use of zebrafish (Danio rerio). Eugene, OR:. University of Oregon Press.
83. Kwan KM, Fujimoto E, Grabher C, Mangum BD, Hardy ME, et al. (2007) The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. Dev Dyn 236: 3088-3099.