Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-10T15:03:59.218Z Has data issue: false hasContentIssue false
  • English
  • Français

Cellular correlates of proneural and notch-delta gene expression in the regenerating zebrafish retina

Published online by Cambridge University Press:  06 September 2007

PATRICK YURCO  and
DAVID A. CAMERON
PATRICK YURCO
Affiliation:
Department of Neuroscience and Physiology, SUNY Upstate Medical University, Syracuse, New York 1Current Address: Department of Biology, LeMoyne College, 1419 Salt Spring Road, Syracuse, NY 13214.
DAVID A. CAMERON
Affiliation:
Department of Neuroscience and Physiology, SUNY Upstate Medical University, Syracuse, New York
Get access Rights & Permissions [Opens in a new window]

Abstract

Fish can regenerate retinal neurons following ocular injury. Evidence is mounting that astrocytic glia function as inducible, regenerative stem cells in this process, but the underlying molecular events that enable neuronal regeneration are comparatively unclear. In the current study gene array, quantitative real-time PCR, in situ hybridization, and immunohistochemical approaches were used to identify, in the damaged retina of adult zebrafish, correlations between transcriptional events and entry into the cell cycle by Müller cells, a type of astrocytic cell present in all vertebrate retinas that is a candidate ‘stem cell’ of regenerated neurons. A proneural gene (achaete-scute homolog 1a, ash1a) and neurogenic components of the Notch signaling pathway, including notch3 and deltaA, were implicated. An injury-induced, enhanced expression of ash1a was observed in Müller cells, which is hypothesized to contribute to the transition of these cells, or their cellular progeny, into a notch3-expressing, regenerative progenitor. A model of vertebrate retinal repair is suggested in which damage-induced expression of proneural genes, plus canonical Notch-Delta signaling, could contribute to retinal stem cell promotion and subsequent regenerative neurogenesis.

Keywords

RegenerationRetinaGene expressionZebrafishNotch
Type
Research Article
Information
Visual Neuroscience , Volume 24 , Issue 3 , May 2007 , pp. 437 - 443
Copyright
© 2007 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Alvarez-Buylla, A. & Lim, D.A. (2004). For the long run: Maintaining germinal niches in the adult brain. Neuron 41, 683–686.CrossRefGoogle Scholar
Asch, W.S., Leake, D., Canger, A.K., Passini, M.A., Argenton, F. & Schechter, N. (1998). Cloning of zebrafish neurofilament cDNAs for plastic in and gefiltin: Increased mRNA expression in ganglion cells after optic nerve injury. Journal of Neurochemistry 71, 20–32.Google Scholar
Austin, C.P., Feldman, D.E., Ida, Jr., J.A. & Cepko, C.L. (1995). Vertebrate retinal ganglion cells are selected from competent progenitors by the action of Notch. Development 121, 3637–3650.Google Scholar
Bernardos, R.L., Lentz, S.I., Wolfe, M.S. & Raymond, P.A. (2005). Notch-Delta signaling is required for spatial patterning and Muller glia differentiation in the zebrafish retina. Developmental Biology 278, 381–395.CrossRefGoogle Scholar
Bertrand, N., Castro, D.S. & Guillemot, F. (2002). Proneural genes and the specification of neural cell types. Nature Neuroscience 3, 517–529.CrossRefGoogle Scholar
Buffo, A., Vosko, M.R., Erturk, D., Hamann, G.F., Jucker, M., Rowitch, D. & Gotz, M. (2005). Expression pattern of the transcription factor Olig2 in response to brain injuries: Implications for neuronal repair. Proceedings of the National Academy of Sciences USA 102, 18183–18188.CrossRefGoogle Scholar
Cameron, D.A. & Easter, Jr., S.S. (1995). Cone photoreceptor regeneration in adult fish retina: Phenotypic determination and mosaic pattern formation. Journal of Neuroscience 15, 2255–2271.Google Scholar
Cameron, D.A., Gentile, K.L., Middleton, F.A. & Yurco, P. (2005). Gene expression profile of intact and regenerating zebrafish retina. Molecular Vision 11, 775–791.Google Scholar
Campuzano, S. & Modolell, J. (1992). Patterning of the Drosophila nervous system: The achaete-scute gene complex. Trends in Genetics 8, 202–208.CrossRefGoogle Scholar
Chitnis, A., Henrique, D., Lewis, J., Ish-Horowicz, D. & Kintner, C. (1995). Primary neurogenesis in Xenopus embryos regulated by a homologue of the Drosophila neurogenic gene Delta. Nature 375, 761–766.CrossRefGoogle Scholar
Doetsch, F., Caille, I., Lim, D.A., Garcia-Verdugo, J.M. & Alvarez-Buylla, A. (1999). Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 9, 703–716.CrossRefGoogle Scholar
Doetsch, F. (2003). The glial identity of neural stem cells. Nature Neuroscience 6, 1127–1134.CrossRefGoogle Scholar
Dorsky, R.I., Chang, W.S., Rapaport, D.H. & Harris, W.A. (1997). Regulation of neuronal diversity in the Xenopus retina by Delta signaling. Nature 385, 67–70.CrossRefGoogle Scholar
Emsley, J.G., Mitchell, B.D., Kempermann, G. & Macklis, J.D. (2005). Adult neurogenesis and repair of the adult CNS with neural progenitors, precursors, and stem cells. Progress in Neurobiology 75, 321–341.CrossRefGoogle Scholar
Ever, L. & Gaiano, N. (2005). Radial ‘glial’ progenitors: Neurogenesis and signaling. Current Opinion in Neurobiology 15, 29–33.CrossRefGoogle Scholar
Fausett, B.V. & Goldman, D. (2006). A role for alpha1 tubulin-expressing Müller glia in regeneration of the injured zebrafish retina. Journal of Neuroscience 26, 6303–6313.Google Scholar
Fischer, A.J. & Reh, T.A. (2001). Müller glia are a potential source of neural regeneration in the post-natal chick retina. Nature Neuroscience 4, 247–252.CrossRefGoogle Scholar
Fischer, A.J. & Reh, T.A. (2003). Potential of Muller glia to become neurogenic retinal progenitor cells. Glia 43, 70–76.CrossRefGoogle Scholar
Garcia, M. & Vecino, E. (2003). Role of Müller glia in neuroprotection and regeneration in the retina. Histology and Histopathology 18, 1205–1218.Google Scholar
Goldman, S. (2003). Glia as neural progenitor cells. Trends in Neuroscience 26, 590–596.CrossRefGoogle Scholar
Haddon, C., Smithers, L., Schneider-Maunoury, S., Coche, T., Henrique, D. & Lewis, J. (1998). Multiple delta genes and lateral inhibition in zebrafish primary neurogenesis. Development 125, 359–370.Google Scholar
Hagg, T. (2005). Molecular regulation of adult CNS neurogenesis: An integrated view. Trends in Neuroscience 28, 589–595.CrossRefGoogle Scholar
Hitchcock, P.F., Lindsey-Myhr, K.J., Easter, Jr., S.S., Mangione-Smith, R. & Jones, D.D. (1992). Local regeneration in the retina of the goldfish. Journal of Neurobiology 23, 187–203.CrossRefGoogle Scholar
Levine, E.M., Hitchcock, P.F., Glasglow, E. & Schecter, N. (1994). Restricted expression of a new paired-class homeobox gene in normal and regenerating adult goldfish retina. Journal of Comparative Neurology 348, 596–606.CrossRefGoogle Scholar
Liu, Q., Londraville, R.L., Azodi, E., Babb, S.G., Chiappini-Williamson, C., Marris, J.A. & Raymond, P.A. (2002). Up-regulation of cadherin-2 and cadherin-4 in regenerating visual structures of adult zebrafish. Experimental Neurology 177, 396–406.CrossRefGoogle Scholar
Ming, G.L. & Song, H. (2005). Adult neurogenesis in the mammalian central nervous system. Annual Review of Neuroscience 28, 223–250.CrossRefGoogle Scholar
Mori, T., Buffo, A. & Gotz, M. (2005). The novel roles of glial cells revisited: The contribution of radial glia and astrocytes to neurogenesis. Current Topics in Developmental Biology 69, 67–99.CrossRefGoogle Scholar
Otteson, D.C. & Hitchcock, P.F. (2003). Stem cells in the teleost fish: Persistent neurogenesis and injury-induced regeneration. Vision Research 43, 927–936.CrossRefGoogle Scholar
Raymond, P.A. & Hitchcock, P.F. (2000). How the neural retina regenerates. Results and Problems in Cell Differentiation 31, 197–218.CrossRefGoogle Scholar
Raymond, P.A., Barthel, L.K., Bernardos, R.L. & Perkowski, J.J. (2006). Molecular characterization of retinal stem cells and their niches in zebrafish retina. BioMed Central Developmental Biology 6, 36.Google Scholar
Reh, T.A. & Levine, E.M. (1998). Multipotential stem cells and progenitors in the vertebrate retina. Journal of Neurobiology 36, 206–220.3.0.CO;2-5>CrossRefGoogle Scholar
Scheer, N., Groth, A., Hans, S. & Campos-Ortega, J.A. (2001). An instructive function for Notch in promoting gliogenesis in the zebrafish retina. Development 128, 1099–1107.Google Scholar
Senut, M.C., Gulati-Leekha, A. & Goldman, D. (2004). An element in the alpha1-tubulin promoter is necessary for retinal expression during optic nerve regeneration but not after eye injury in the adult zebrafish. Journal of Neuroscience 24, 7663–7673.Google Scholar
Seri, B., Garcia-Verdugo, J.M., McEwen, B.S. & Alarez-Buylla, A. (2001). Astrocytes give rise to new neurons in the adult mammalian hippocampus. Journal of Neuroscience 21, 7153–7160.Google Scholar
Shimamura, K., Hirano, S., McMahon, A.P. & Takeichi, M. (1994). Wnt-1-dependent regulation of local E-cadherin and alpha N-catenin expression in the embryonic mouse brain. Development 120, 2225–2234.Google Scholar
Stenkamp, D.L. & Cameron, D.A. (2002). Cellular pattern formation in the retina: Retinal regeneration as a model system. Molecular Vision 8, 280–293.Google Scholar
Sullivan, S.A., Barthel, L.K., Largent, B.L. & Raymond, P.A. (1997). A goldfish Notch-3 homologue is expressed in neurogenic regions of embryonic, adult, and regenerating brain and retina. Developmental Genetics 20, 208–223.3.0.CO;2-B>CrossRefGoogle Scholar
Tamamaki, N., Nakamura, K., Okamoto, K. & Ogawa, M. (2001). Radial glia is a progenitor of neocortical neurons in the developing cerebral cortex. Neuroscience Research 41, 51–60.CrossRefGoogle Scholar
Viczian, A.S., Vignali, R., Zuber, M.E., Barsacchi, G. & Harris, W.A. (2003). XOtx5b and XOtx2 regulate photoreceptor and bipolar fates in the Xenopus retina. Development 130, 1281–1294.Google Scholar
Vihtelic, T.S. & Hyde, D.R. (2000). Light-induced rod and cone cell death and regeneration in the adult albino zebrafish (Danio rerio) retina. Journal of Neurobiology 44, 289–307.3.0.CO;2-H>CrossRefGoogle Scholar
Vihtelic, T.S., Soverly, J.E., Kassen, S.C. & Hyde, D.R. (2006). Retinal regional differences in photoreceptor cell death and regeneration in light-lessoned albino zebrafish. Experimental Eye Research 82, 558–575.CrossRefGoogle Scholar
Wu, D.M., Schneiderman, T., Burgett, J., Gokhale, P., Barthel, L. & Raymond, P.A. (2001). Cones regenerate from retinal stem cells sequestered in the inner nuclear layer of adult goldfish retina. Investigative Ophthalmology and Visual Science 42, 2115–2124.Google Scholar
Yoon, K. & Gaiano, N. (2005). Notch signaling in the mammalian central nervous system: Insights from mouse mutants. Nature Neuroscience 8, 709–715.CrossRefGoogle Scholar
Yurco, P. & Cameron, D.A. (2005). Responses of Muller glia to retinal injury in adult zebrafish. Vision Research 45, 991–1002.CrossRefGoogle Scholar