Ganglion cell regeneration following whole-retina destruction in zebrafish
Open accessAbstract
The retinas of adult teleost fish can regenerate neurons following injury. The current study provides the first documentation of functional whole retina regeneration in the zebrafish, Danio rerio , following intraocular injection of the cytotoxin, ouabain. Loss and replacement of laminated retinal tissue was monitored by analysis of cell death and cell proliferation, and by analysis of retina‐specific gene expression patterns. The spatiotemporal process of retinal ganglion cell (RGC) regeneration was followed through the use of selective markers, and was found to largely recapitulate the spatiotemporal process of embryonic ganglion cell neurogenesis, over a more protracted time frame. However, the re‐expression of some ganglion cell markers was not observed. The growth and pathfinding of ganglion cell axons was evaluated by measurement of the optic nerve head (ONH), and the restoration of normal ONH size was found to correspond to the time of recovery of two visually‐mediated behaviors. However, some abnormalities were noted, including overproduction of RGCs, and progressive and excessive growth of the ONH at longer recovery times. This model system for whole‐retina regeneration has provided an informative view of the regenerative process. © 2007 Wiley Periodicals, Inc. Develop Neurobiol, 2008
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Teleost fish such as zebrafish can regenerate a damaged retina and restore sight.
“In contrast, teleost fish, like zebrafish exhibit a remarkable regenerative ability that can restore sight to a damaged retina (Lindsey and Powers, 2007; Mensinger and Powers, 1999; Sherpa et al., 2008).”
From Retinal injury, growth factors, and cytokines converge on β-catenin and pStat3 signaling to stimulate retina regeneration (2014) · cites this paper as Sherpa et al., 2008
Cites
The zebrafish book : a guide for the laboratory use of zebrafish (Danio rerio)
Westerfield, M. (1995) · Medical Entomology and Zoology · Cited by 6,813 · see citing works
Retinal Stem Cells in the Adult Mammalian Eye
Tropepe, V., Coles, B. L. K., Chiasson, B. J., Horsford, D. J., Elia, A., McInnes, R. R., & van der Kooy, D. (2000) · Science · doi:10.1126/science.287.5460.2032 · Cited by 1,085 · see citing works
Bernardos, R. L., Barthel, L. K., Meyers, J. R., & Raymond, P. A. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.1624-07.2007 · Cited by 647 · see citing works
Müller glia are a potential source of neural regeneration in the postnatal chicken retina
Fischer, A. J., & Reh, T. A. (2001) · Nature Neuroscience · doi:10.1038/85090 · Cited by 579 · see citing works
Molecular characterization of retinal stem cells and their niches in adult zebrafish
Raymond, P. A., Barthel, L. K., Bernardos, R. L., & Perkowski, J. J. (2006) · BMC Developmental Biology · doi:10.1186/1471-213x-6-36 · Cited by 504 · see citing works
A Role for 1 Tubulin-Expressing Muller Glia in Regeneration of the Injured Zebrafish Retina
Fausett, B. V., & Goldman, D. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.0332-06.2006 · Cited by 435 · see citing works
Identification of Neural Progenitors in the Adult Mammalian Eye
Ahmad, I., Tang, L., & Pham, H. (2000) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.2000.2473 · Cited by 433 · see citing works
Retinal Ganglion Cell Genesis Requires lakritz, a Zebrafish atonal Homolog
Kay, J. N., Finger‐Baier, K., Roeser, T., Staub, W., & Baier, H. (2001) · Neuron · doi:10.1016/s0896-6273(01)00312-9 · Cited by 417 · see citing works
Patterning of the Zebrafish Retina by a Wave of Sonic Hedgehog Activity
Neumann, C. J., & Nuesslein-Volhard, C. (2000) · Science · doi:10.1126/science.289.5487.2137 · Cited by 385 · see citing works
Retinal Neurogenesis: The Formation of the Initial Central Patch of Postmitotic Cells
Hu, M., & Easter, S. S. (1999) · Developmental Biology · doi:10.1006/dbio.1998.9031 · Cited by 364 · see citing works
Improved method for obtaining 3-microns cryosections for immunocytochemistry.
Barthel, L. K., & Raymond, P. A. (1990) · Journal of Histochemistry & Cytochemistry · doi:10.1177/38.9.2201738 · Cited by 317 · see citing works
Zebrafish elav/HuC homologue as a very early neuronal marker
Kim, C., Ueshima, E., Muraoka, O., Tanaka, H., Yeo, S., Huh, T., & Miki, N. (1996) · Neuroscience Letters · doi:10.1016/0304-3940(96)13021-4 · Cited by 317 · see citing works
Regeneration of inner retinal neurons after intravitreal injection of ouabain in zebrafish
Fimbel, S. M., Montgomery, J. E., Burket, C. T., & Hyde, D. R. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.5317-06.2007 · Cited by 298 · see citing works
Self-citationGenesis of rods in teleost fish retina
Johns, P. R., & Fernald, R. D. (1981) · Nature · doi:10.1038/293141a0 · Cited by 274 · see citing works
Sequence and expression pattern ofpax-6are highly conserved between zebrafish and mice
Püschel, A. W., Gruß, P., & Westerfield, M. (1992) · Development · doi:10.1242/dev.114.3.643 · Cited by 261 · see citing works
Midline Signals Regulate Retinal Neurogenesis in Zebrafish
Masai, I., Stemple, D. L., Okamoto, H., et al. (2000) · Neuron · doi:10.1016/s0896-6273(00)00034-9 · Cited by 206 · see citing works
Kassen, S. C., Ramanan, V., Montgomery, J. E., T. Burket, C., Liu, C., Vihtelic, T. S., & Hyde, D. R. (2007) · Developmental Neurobiology · doi:10.1002/dneu.20362 · Cited by 203 · see citing works
Self-citationRegulation of retinal ganglion cell production by Sonic hedgehog
Zhang, X., & Yang, X.-J. (2001) · Development · doi:10.1242/dev.128.6.943 · Cited by 197 · see citing works
Putative Stem Cells and the Lineage of Rod Photoreceptors in the Mature Retina of the Goldfish
Otteson, D. C., D’Costa, A. R., & Hitchcock, P. F. (2001) · Developmental Biology · doi:10.1006/dbio.2001.0163 · Cited by 195 · see citing works
Gan, L., Wang, S. W., Huang, Z., & Klein, W. H. (1999) · Developmental Biology · doi:10.1006/dbio.1999.9280 · Cited by 190 · see citing works
Mosaics of Islet-1-Expressing Amacrine Cells Assembled by Short-Range Cellular Interactions
Galli‐Resta, L., Resta, G., Tan, S., & Reese, B. E. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-20-07831.1997 · Cited by 190 · see citing works
Raymond, P., & Easter, S. (1983) · Journal of Neuroscience · doi:10.1523/jneurosci.03-05-01077.1983 · Cited by 185 · see citing works
Differentiation of the Vertebrate Retina Is Coordinated by an FGF Signaling Center
Martínez‐Morales, J. R., Bene, F. D., Nica, G., Hammerschmidt, M., Bovolenta, P., & Wittbrodt, J. (2005) · Developmental Cell · doi:10.1016/j.devcel.2005.01.022 · Cited by 182 · see citing works
Responses of Müller glia to retinal injury in adult zebrafish
Yurco, P., & Cameron, D. A. (2004) · Vision Research · doi:10.1016/j.visres.2004.10.022 · Cited by 177 · see citing works
Persistent and injury-induced neurogenesis in the vertebrate retina
Hitchcock, P. F., Ochocinska, M. J., Sieh, A., & Otteson, D. C. (2004) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2004.01.001 · Cited by 174 · see citing works
Nornes, S., Clarkson, M. J., Mikkola, I., Pedersen, M., Bardsley, A., Martı́nez-Barberá, J. P., Krauss, S. J. K., & Johansen, T. (1998) · Mechanisms of Development · doi:10.1016/s0925-4773(98)00156-7 · Cited by 171 · see citing works
Regeneration of goldfish retina: Rod precursors are a likely source of regenerated cells
Raymond, P. A., Reifler, M. J., & Rivlin, P. K. (1988) · Journal of Neurobiology · doi:10.1002/neu.480190504 · Cited by 170 · see citing works
Neurogenesis in the visual system of embryonic and adult zebrafish (Danio rerio)
Marcus, R. C., Delaney, C. L., & Easter, S. S. (1999) · Visual Neuroscience · doi:10.1017/s095252389916303x · Cited by 164 · see citing works
Li, L., & Dowling, J. E. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.21.11645 · Cited by 161 · see citing works
Self-citationGerminal cells in the goldfish retina that produce rod photoreceptors
Raymond, P. A., & Rivlin, P. K. (1987) · Developmental Biology · doi:10.1016/0012-1606(87)90338-1 · Cited by 159 · see citing works
Birth and fate of proliferative cells in the inner nuclear layer of the mature fish retina
Julian, D. A., Ennis, K., & Korenbrot, J. I. (1998) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19980511)394:3 · Cited by 154 · see citing works
Wu, D. M., Schneiderman, T. E., Burgett, J., Gokhale, P. J., Barthel, L., & Raymond, P. A. (2001) · PubMed · Cited by 141 · see citing works
Local regeneration in the retina of the goldfish
Hitchcock, P. F., Myhr, K. L., Easter, S. S., et al. (1992) · Journal of Neurobiology · doi:10.1002/neu.480230209 · Cited by 134 · see citing works
Wang, S. W., Mu, X., Bowers, W. J., Kim, D.-S., Plas, D. T., Crair, M. C., Federoff, H. J., Gan, L., & Klein, W. H. (2002) · Development · doi:10.1242/dev.129.2.467 · Cited by 134 · see citing works
Neurogenesis in the Fish Retina
Stenkamp, D. L. (2007) · International review of cytology · doi:10.1016/s0074-7696(06)59005-9 · Cited by 128 · see citing works
Self-citationZebrafish visual sensitivity is regulated by a circadian clock
Li, L., & Dowling, J. E. (1998) · Visual Neuroscience · doi:10.1017/s0952523898155050 · Cited by 122 · see citing works
Self-citationSelective regeneration of photoreceptors in goldfish retina
Braisted, J. E., Essman, T. F., & Raymond, P. A. (1994) · Development · doi:10.1242/dev.120.9.2409 · Cited by 119 · see citing works
Mu, X., Beremand, P. D., Zhao, S., Pershad, R., Sun, H., Scarpa, A., Liang, S., Thomas, T. L., & Klein, W. H. (2004) · Development · doi:10.1242/dev.01010 · Cited by 115 · see citing works
Cellular proliferation and neurogenesis in the injured retina of adult zebrafish
CAMERON, D. A. (2000) · Visual Neuroscience · doi:10.1017/s0952523800175121 · Cited by 115 · see citing works
Robb, L. G., Mifsud, L., Hartley, L., Biben, C., Copeland, N. G., Gilbert, D. J., Jenkins, N. A., & Harvey, R. P. (1998) · Developmental Dynamics · doi:10.1002/(sici)1097-0177(199809)213:1 · Cited by 113 · see citing works
Regeneration of the goldfish retina after exposure to different doses of ouabain
Maier, W. A., III, & Wolburg, H. (1979) · Cell and Tissue Research · doi:10.1007/bf00239223 · Cited by 110 · see citing works
A gene regulatory hierarchy for retinal ganglion cell specification and differentiation
Mu, X., & Klein, W. H. (2004) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2003.09.009 · Cited by 110 · see citing works
Stenkamp, D. L., & Frey, R. A. (2003) · Developmental Biology · doi:10.1016/s0012-1606(03)00121-0 · Cited by 98 · see citing works
Self-citationOnset and time course of apoptosis in the developing zebrafish retina
Biehlmaier, O., Neuhauss, S. C. F., & Köhler, K. (2001) · Cell and Tissue Research · doi:10.1007/s004410100447 · Cited by 98 · see citing works
Levine, E. M., Hitchcock, P. F., Glasgow, E. F., et al. (1994) · The Journal of Comparative Neurology · doi:10.1002/cne.903480409 · Cited by 89 · see citing works
Gene expression profiles of intact and regenerating zebrafish retina.
Cameron, D. A., Gentile, K. L., Middleton, F. A., & Yurco, P. (2005) · PubMed · Cited by 82 · see citing works
Harzsch, S., & Dawirs, R. R. (1996) · Journal of Neurobiology · doi:10.1002/(sici)1097-4695(199603)29:3 · Cited by 79 · see citing works
Barthel, L. K., & Raymond, P. A. (1993) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(93)90002-9 · Cited by 75 · see citing works
Cytodifferentiation of photoreceptors in larval goldfish: Delayed maturation of rods
Raymond, P. A. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902360108 · Cited by 66 · see citing works
Mi, Z. P., Jiang, P., Weng, W., Lindberg, F. P., Narayanan, V., & Lagenaur, C. F. (2000) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(20000117)416:3 · Cited by 65 · see citing works
Visual function in regenerating teleost retina following cytotoxic lesioning
MENSINGER, A. F., & POWERS, M. K. (1999) · Visual Neuroscience · doi:10.1017/s0952523899162059 · Cited by 63 · see citing works
Sullivan, S. A., Barthel, L. K., Largent, B. L., & Raymond, P. A. (1997) · Developmental Genetics · doi:10.1002/(sici)1520-6408(1997)20:3 · Cited by 57 · see citing works
Function of Neurolin (DM-GRASP/SC-1) in Guidance of Motor Axons during Zebrafish Development
Ott, H., Diekmann, H., Stuermer, C. A. O., et al. (2001) · Developmental Biology · doi:10.1006/dbio.2001.0278 · Cited by 56 · see citing works
AL‐SHAMMA, H. A., & Vries, G. J. D. (1996) · Journal of Neurobiology · doi:10.1002/(sici)1097-4695(199601)29:1 · Cited by 45 · see citing works
Up-regulation of Cadherin-2 and Cadherin-4 in Regenerating Visual Structures of Adult Zebrafish
Liu, Q., Londraville, R. L., Azodi, E., Clendenon, S. G., Chiappini-Williamson, C., Marrs, J. A., & Raymond, P. A. (2002) · Experimental Neurology · doi:10.1006/exnr.2002.8008 · Cited by 43 · see citing works
Axonal Transport, Degeneration, and Regeneration in the Visual System of the Goldfish
Wolburg, H. (1981) · Advances in anatomy, embryology and cell biology · doi:10.1007/978-3-642-67801-1 · Cited by 40 · see citing works
deCarvalho, A. C., Cappendijk, S. L. T., & Fadool, J. M. (2004) · Developmental Dynamics · doi:10.1002/dvdy.10475 · Cited by 40 · see citing works
Silver, P. H. (1974) · Vision Research · doi:10.1016/0042-6989(74)90091-1 · Cited by 28 · see citing works
Wolburg, H. (1981) · Advances in anatomy, embryology and cell biology · doi:10.1007/978-3-642-67801-1_1 · Cited by 28 · see citing works
Kästner, R., & Wolburg, H. (1982) · Zeitschrift für Naturforschung C · doi:10.1515/znc-1982-11-1229 · Cited by 18 · see citing works
Time- and dose-dependent influence of ouabain on the ultrastructure of optic neurones
Wolburg, H. (1975) · Cell and Tissue Research · doi:10.1007/bf00219941 · Cited by 15 · see citing works
Stuermer, C. A. O., Niepenberg, A., & Wolburg, H. (1985) · Neuroscience Letters · doi:10.1016/0304-3940(85)90076-x · Cited by 14 · see citing works
Metabolic activity in optic tectum during regeneration of retina in adult goldfish
Melzer, P., & Powers, M. K. (2001) · Visual Neuroscience · doi:10.1017/s0952523801184099 · Cited by 8 · see citing works
Haamedi, S. N., Karten, H. J., & Djamgoz, M. B. A. (2001) · The Journal of Comparative Neurology · doi:10.1002/1096-9861(20010319)431:4 · Cited by 8 · see citing works
A new metachromatic stain technique for paraffin‐embedded neural tissue using thionin
Eichler, V. B., & Taylor, P. W. (1976) · Journal of Microscopy · doi:10.1111/j.1365-2818.1976.tb01083.x · Cited by 6 · see citing works
Fashena, D. (1999) · doi:10.1002/(sici)1096-9861(19990412)406:3
Vihtelic, T. S., & Hyde, D. R. (2000) · Journal of Neurobiology · doi:10.1002/1097-4695(20000905)44:3
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Ramachandran, R., Zhao, X.-F., & Goldman, D. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1107220108 · Cited by 206 · see citing works
Montgomery, J. E., Parsons, M. J., & Hyde, D. R. (2010) · Journal of Comparative Neurology · doi:10.1002/cne.22243 · Cited by 161 · see citing works
Self-citationWan, J., Zhao, X.-F., Vojtek, A., & Goldman, D. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.08.048 · Cited by 143 · see citing works
“In contrast, teleost fish, like zebrafish exhibit a remarkable regenerative ability that can restore sight to a damaged retina (Lindsey and Powers, 2007; Mensinger and Powers, 1999; Sherpa et al., 2008).”
BackgroundNelson, C. M., Gorsuch, R. A., Bailey, T. J., Ackerman, K. M., Kassen, S. C., & Hyde, D. R. (2012) · Journal of Comparative Neurology · doi:10.1002/cne.23213 · Cited by 123 · see citing works
Self-citationKassen, S. C., Thummel, R., Campochiaro, L. A., Harding, M. J., Bennett, N. A., & Hyde, D. R. (2009) · Experimental Eye Research · doi:10.1016/j.exer.2009.01.007 · Cited by 116 · see citing works
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- Authors
- Sherpa, T., Fimbel, S. M., Mallory, D. E., Maaswinkel, H., Spritzer, S. D., Sand, J. A., Li, L., Hyde, D. R., & Stenkamp, D. L.
- Affiliations
- University of Notre Dame (US)
- University of Idaho (US)
- Corresponding author
- Stenkamp, Deborah L.
- Venue
- Developmental Neurobiology
- Publisher
- Wiley
- Published
- 2007-11-13
- Volume
- 68
- Issue
- 2
- Pages
- 166-181
- ISSN
- 1932-8451 (ISSN-L)
- 1932-846X
- PMC
- PMC2581885
- OpenAlex
- W2085375111
- Cited by
- 174
- References
- 67
- Citations by year
- 2026: 10 · 2025: 9 · 2024: 7 · 2023: 15 · 2022: 14 · 2021: 11 · 2020: 9 · 2019: 11 · 2018: 19 · 2017: 8 · 2016: 2 · 2015: 6 · 2014: 11 · 2013: 11 · 2012: 6
- FWCI
- 2.12
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Developmental Neurobiology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (1s10od018044-01)
- National Eye Institute (R01EY012146)
- National Center for Research Resources (P20RR016454)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Retinal Development and Disorders
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Zebrafish Biomedical Research Applications
- Keywords
- retinal ganglion cell regeneration, zebrafish, ouabain, retinal damage, optic nerve head, axon guidance, cell proliferation, cell death, retinal neurogenesis
- MeSH terms
- Animals, Behavior, Animal, Biological Assay, Bromodeoxyuridine, Denervation, Nerve Regeneration, Neurotoxins, Optic Disk, Ouabain, Retinal Ganglion Cells, Time Factors, Vision, Ocular, Zebrafish, Biomarkers, Cell Death, Gene Expression Regulation, Developmental, Proliferating Cell Nuclear Antigen, Recovery of Function, Growth Cones, Cell Proliferation
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