Molecular characterization of retinal stem cells and their niches in adult zebrafish
Open accessAbstract
Background: The persistence in adult teleost fish of retinal stem cells that exhibit all of the features of true 'adult stem cells' – self-renewal, multipotency, and the capacity to respond to injury by mitotic activation with the ability to regenerate differentiated tissues – has been known for several decades. However, the specialized cellular and molecular characteristics of these adult retinal stem cells and the microenvironmental niches that support their maintenance in the differentiated retina and regulate their activity during growth and regeneration have not yet been elucidated. Results: Our data show that the zebrafish retina has two kinds of specialized niches that sustain retinal stem cells: 1) a neuroepithelial germinal zone at the interface between neural retina and ciliary epithelium, called the ciliary marginal zone (CMZ), a continuous annulus around the retinal circumference, and 2) the microenvironment around some Müller glia in the differentiated retina. In the uninjured retina, scattered Müller glia (more frequently those in peripheral retina) are associated with clusters of proliferating retinal progenitors that are restricted to the rod photoreceptor lineage, but following injury, the Müller-associated retinal progenitors can function as multipotent retinal stem cells to regenerate other types of retinal neurons. The CMZ has several features in common with the neurogenic niches in the adult mammalian brain, including access to the apical epithelial surface and a close association with blood vessels. Müller glia in the teleost retina have a complex response to local injury that includes some features of reactive gliosis (up-regulation of glial fibrillary acidic protein, GFAP, and re-entry into the cell cycle) together with dedifferentiation and re-acquisition of phenotypic and molecular characteristics of multipotent retinal progenitors in the CMZ (diffuse distribution of N-cadherin, activation of Notch-Delta signaling, and expression of rx1, vsx2/Chx10, and pax6a) along with characteristics associated with radial glia (expression of brain lipid binding protein, BLBP). We also describe a novel specific marker for Müller glia, apoE. Conclusion: The stem cell niches that support multi-lineage retinal progenitors in the intact, growing and regenerating teleost retina have properties characteristic of neuroepithelia and neurogenic radial glia. The regenerative capacity of the adult zebrafish retina with its ability to replace lost retinal neurons provides an opportunity to discover the molecular regulators that lead to functional repair of damaged neural tissue.
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Notch signaling components are induced in the injured adult zebrafish retina.
“Notch signaling components are also induced in the injured adult zebrafish retina”
From HB-EGF is Necessary and Sufficient for Müller Glia Dedifferentiation and Retina Regeneration (2012) · cites this paper as Raymond et al., 2006
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Fgf signaling is required for photoreceptor maintenance in the adult zebrafish retina
Hochmann, S., Kaslin, J., Hans, S., Weber, A., Machate, A., Geffarth, M., Funk, R. H. W., & Brand, M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0030365 · Cited by 62 · see citing works
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- Authors
- Raymond, P. A., Barthel, L. K., Bernardos, R. L., & Perkowski, J. J.
- Affiliations
- University of Michigan (US)
- Corresponding author
- Raymond, Pamela A
- Barthel, Linda K
- Bernardos, Rebecca L
- Perkowski, John J
- Venue
- BMC Developmental Biology
- Published
- 2006-07-26
- Volume
- 6
- Issue
- 1
- Pages
- 36-36
- ISSN
- 1471-213X (ISSN-L)
- PMC
- PMC1564002
- OpenAlex
- W2162463187
- Cited by
- 504
- References
- 100
- Citations by year
- 2026: 8 · 2025: 20 · 2024: 19 · 2023: 22 · 2022: 26 · 2021: 29 · 2020: 29 · 2019: 23 · 2018: 37 · 2017: 24 · 2016: 25 · 2015: 23 · 2014: 22 · 2013: 31 · 2012: 29
- FWCI
- 10.32
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- BMC Developmental Biology (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Deep Blue (University of Michigan) (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Funders
- National Institutes of Health (NIH T32, NIH-R01)
- National Eye Institute (R01EY004318, T32EY013934)
- National Institute on Deafness and Other Communication Disorders (T32 DC05341, T32DC005341)
- National Institute of Neurological Disorders and Stroke (F31NS047909, T32NS076401)
- 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 stem cells, zebrafish retina, ciliary marginal zone, Müller cells, stem cell niche, retinal regeneration, reactive gliosis, dedifferentiation, Delta-Notch signaling, radial glia, apolipoprotein E, glial fibrillary acidic protein, self-renewal, multipotency, teleosts
- MeSH terms
- Aging, Animals, Cell Differentiation, Retina, Stem Cells, Zebrafish, In Situ Hybridization, Gene Expression Regulation, Developmental, Zebrafish Proteins, Cell Proliferation
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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