Notch and Wnt signaling mediated rod photoreceptor regeneration by Müller cells in adult mammalian retina
Open accessAbstract
BACKGROUND: Evidence emerging from a variety of approaches used in different species suggests that Müller cell function may extend beyond its role of maintaining retinal homeostasis to that of progenitors in the adult retina. Enriched Müller cells in vitro or those that re-enter cell cycle in response to neurotoxin-damage to retina in vivo display multipotential and self-renewing capacities, the cardinal features of stem cells. METHODOLOGY/PRINCIPAL FINDINGS: We demonstrate that Notch and Wnt signaling activate Müller cells through their canonical pathways and that a rare subset of activated Müller cells differentiates along rod photoreceptor lineage in the outer nuclear layer. The differentiation of activated Müller cells along photoreceptor lineage is confirmed by multiple approaches that included Hoechst dye efflux analysis, genetic analysis using retina from Nrl-GFP mice, and lineage tracing using GS-GFP lentivirus in wild type and rd mice in vitro and S334ter rats in vivo. Examination of S334ter rats for head-neck tracking of visual stimuli, a behavioral measure of light perception, demonstrates a significant improvement in light perception in animals treated to activate Müller cells. The number of activated Müller cells with rod photoreceptor phenotype in treated animals correlates with the improvement in their light perception. CONCLUSION/SIGNIFICANCE: In summary, our results provide a proof of principle for non-neurotoxin-mediated activation of Müller cells through Notch and Wnt signaling toward the regeneration of rod photoreceptors.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Notch signaling stimulates proliferation of Müller glia-derived progenitors in birds and mammals.
“Notch signaling stimulated proliferation of MG-derived progenitors in birds and mammals”
From HB-EGF is Necessary and Sufficient for Müller Glia Dedifferentiation and Retina Regeneration (2012) · cites this paper as Del Debbio et al., 2010
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
SOX2 Functions to Maintain Neural Progenitor Identity
Graham, V., Khudyakov, J. I., Ellis, P., & Pevny, L. (2003) · Neuron · doi:10.1016/s0896-6273(03)00497-5 · Cited by 1,344 · see citing works
Álvarez-Buylla, A., & Lim, D. A. (2004) · Neuron · doi:10.1016/s0896-6273(04)00111-4 · Cited by 1,320 · see citing works
Retinal repair by transplantation of photoreceptor precursors
MacLaren, R. E., Pearson, R. A., MacNeil, A., Douglas, R. H., Salt, T. E., Akimoto, M., Swaroop, A., Sowden, J. C., & Ali, R. R. (2006) · Nature · doi:10.1038/nature05161 · Cited by 1,099 · see citing works
Goodell, M. A., Rosenzweig, M., Kim, H. L., Marks, D. F., DeMaria, M., Paradis, G. A., Grupp, S. A., Sieff, C. A., Mulligan, R. C., & Johnson, R. P. (1997) · Nature Medicine · doi:10.1038/nm1297-1337 · Cited by 1,086 · see citing works
Nrl is required for rod photoreceptor development
Mears, A. J., Kondo, M., Swain, P. K., Takada, Y., Bush, R. A., Saunders, T. L., Sieving, P. A., & Swaroop, A. (2001) · Nature Genetics · doi:10.1038/ng774 · Cited by 912 · see citing works
Glial cells generate neurons: the role of the transcription factor Pax6
Heins, N., Malatesta, P., Cecconi, F., Nakafuku, M., Tucker, K. L., Hack, M. A., Chapouton, P., Barde, Y.-A., & Götz, M. (2002) · Nature Neuroscience · doi:10.1038/nn828 · Cited by 775 · 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
rax, Hes1, and notch1 promote the formation of Müller glia by postnatal retinal progenitor cells.
Furukawa, T., Mukherjee, S., Bao, Z., Morrow, E. M., & Cepko, C. (2000) · Neuron · doi:10.1016/s0896-6273(00)81171-x · Cited by 545 · see citing works
A side order of stem cells: the SP phenotype
Challen, G. A., & Little, M. H. (2006) · Stem Cells · doi:10.1634/stemcells.2005-0116 · Cited by 475 · see citing works
Potential for neural regeneration after neurotoxic injury in the adult mammalian retina
Ooto, S., Akagi, T., Kageyama, R., Akita, J., Mandai, M., Honda, Y., & Takahashi, M. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0402129101 · Cited by 454 · see citing works
Control of Müller glial cell proliferation and activation following retinal injury
Dyer, M. A., & Cepko, C. L. (2000) · Nature Neuroscience · doi:10.1038/78774 · Cited by 442 · 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
Hes binding to STAT3 mediates crosstalk between Notch and JAK–STAT signalling
Kamakura, S., Oishi, K., Yoshimatsu, T., Nakafuku, M., Masuyama, N., & Gotoh, Y. (2004) · Nature Cell Biology · doi:10.1038/ncb1138 · Cited by 424 · see citing works
Molecular basis of transdifferentiation of pancreas to liver
Shen, C., Slack, J. M. W., & Tosh, D. (2000) · Nature Cell Biology · doi:10.1038/35046522 · Cited by 403 · see citing works
Liao, Y.-F., Wang, B.-J., Cheng, H.-T., Kuo, L.-H., & Wolfe, M. S. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m402034200 · Cited by 389 · see citing works
Timing and topography of cell genesis in the rat retina
Rapaport, D. H., Wong, L., Wood, E. D., Yasumura, D., & LaVail, M. M. (2004) · The Journal of Comparative Neurology · doi:10.1002/cne.20134 · Cited by 376 · see citing works
Differential regulation of midbrain dopaminergic neuron development by Wnt-1, Wnt-3a, and Wnt-5a
Castelo‐Branco, G., Wagner, J., Rodríguez, F. J., Kele, J., Sousa, K. M., Rawal, N., Pasolli, H. A., Fuchs, E. V., Kitajewski, J., & Arenas, E. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1534900100 · Cited by 367 · see citing works
Hsieh, J.-C., Rattner, A., Smallwood, P. M., & Nathans, J. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.7.3546 · Cited by 349 · see citing works
Kohwi, M., Osumi, N., Rubenstein, J. L. R., & Álvarez-Buylla, A. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1435-05.2005 · Cited by 329 · see citing works
Wnt signaling promotes regeneration in the retina of adult mammals
Osakada, F., Ooto, S., Akagi, T., Mandai, M., Akaike, A., & Takahashi, M. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.4193-06.2007 · Cited by 322 · see citing works
Tomita, K., Ishibashi, M., Nakahara, K., Ang, S., Nakanishi, S., Guillemot, F., & Kageyama, R. (1996) · Neuron · doi:10.1016/s0896-6273(00)80093-8 · Cited by 322 · see citing works
Das, A. V., Mallya, K. B., Zhao, X., Ahmad, F., Bhattacharya, S., Thoreson, W. B., Hegde, G. V., & Ahmad, I. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.07.029 · Cited by 297 · see citing works
Self-citationGlial cell fate specification modulated by the bHLH gene Hes5in mouse retina
Hojo, M., Ohtsuka, T., Hashimoto, N., Gradwohl, G., Guillemot, F., & Kageyama, R. (2000) · Development · doi:10.1242/dev.127.12.2515 · Cited by 278 · see citing works
The Proneural Basic Helix-Loop-Helix Gene <i>Ascl1a</i> Is Required for Retina Regeneration
Fausett, B. V., Gumerson, J. D., & Goldman, D. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.4853-07.2008 · Cited by 251 · see citing works
Notch 1 inhibits photoreceptor production in the developing mammalian retina
Jadhav, A. P., Mason, H. A., & Cepko, C. L. (2006) · Development · doi:10.1242/dev.02245 · Cited by 248 · see citing works
Wnt2b controls retinal cell differentiation at the ciliary marginal zone
Kubo, F., Takeichi, M., & Nakagawa, S. (2003) · Development · doi:10.1242/dev.00244 · Cited by 215 · see citing works
Notch signaling promotes astrogliogenesis via direct CSL‐mediated glial gene activation
Ge, W., Martinowich, K., Wu, X., He, F., Miyamoto, A., Fan, G., Weinmaster, G., & Sun, Y. E. (2002) · Journal of Neuroscience Research · doi:10.1002/jnr.10364 · Cited by 203 · see citing works
Hes1 Directly Controls Cell Proliferation through the Transcriptional Repression of p27 Kip1
Murata, K., Hattori, M., Hirai, N., Shinozuka, Y., Hirata, H., Kageyama, R., Sakai, T., & Minato, N. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.10.4262-4271.2005 · Cited by 200 · see citing works
Zhou, C. J., Zhao, C., & Pleasure, S. J. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.4071-03.2004 · Cited by 196 · see citing works
Notch1 modulates timing of G1-S progression by inducing SKP2 transcription and p27Kip1 degradation
Sarmento, L. M., Huang, H., Limón, A., Gordon, W., Fernandes, J., Tavares, M. J., Miele, L., Cardoso, A. A., Classon, M., & Carlesso, N. (2005) · The Journal of Experimental Medicine · doi:10.1084/jem.20050559 · Cited by 191 · see citing works
Poché, R. A., Furuta, Y., Chaboissier, M., Schedl, A., & Behringer, R. R. (2008) · The Journal of Comparative Neurology · doi:10.1002/cne.21746 · Cited by 184 · 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
Liu, C., Li, Y., Peng, M., Laties, A. M., & Wen, R. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-12-04778.1999 · Cited by 166 · see citing works
Diffusible rod-promoting signals in the developing rat retina
Watanabe, T., & RAFF, M. C. (1992) · Development · doi:10.1242/dev.114.4.899 · Cited by 149 · see citing works
Fujimura, N., Taketo, M. M., Mori, M., Kořínek, V., & Kozmík, Z. (2009) · Developmental Biology · doi:10.1016/j.ydbio.2009.07.002 · Cited by 145 · see citing works
α-Aminoadipate Induces Progenitor Cell Properties of Muller Glia in Adult Mice
Takeda, M., Takamiya, A., Jiao, J., Cho, K., Trevino, S. G., Matsuda, T., & Chen, D. F. (2008) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.07-0434 · Cited by 135 · see citing works
Wnt Regulation of Progenitor Maturation in the Cortex Depends on Shh or Fibroblast Growth Factor 2
Viti, J., Gulácsi, A., & Lillien, L. E. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-13-05919.2003 · Cited by 133 · see citing works
Parameswaran, S., Balasubramanian, S., Babai, N. Z., Qiu, F., Eudy, J. D., Thoreson, W. B., & Ahmad, I. (2010) · Stem Cells · doi:10.1002/stem.320 · Cited by 130 · see citing works
Self-citationWeksberg, D. C., Chambers, S. M., Boles, N. C., & Goodell, M. A. (2007) · Blood · doi:10.1182/blood-2007-09-115006 · Cited by 123 · see citing works
Exogenous growth factors induce the production of ganglion cells at the retinal margin
Fischer, A. J., Dierks, B. D., & Reh, T. A. (2002) · Development · doi:10.1242/dev.129.9.2283 · Cited by 118 · see citing works
Differentiation of embryonic stem cells into retinal neurons
Zhao, X., Liu, J., & Ahmad, I. (2002) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(02)02126-5 · Cited by 112 · see citing works
Self-citationInteractions between Fibroblast Growth Factors and Notch Regulate Neuronal Differentiation
Faux, C. H., Turnley, A. M., Epa, R., Cappai, R., & Bartlett, P. F. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-15-05587.2001 · Cited by 111 · see citing works
Neural stem cells in the mammalian eye: types and regulation
Ahmad, I., Das, A. V., James, J., Bhattacharya, S., & Zhao, X. (2004) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2003.09.003 · Cited by 110 · see citing works
Self-citationDirect Identification and Enrichment of Retinal Stem Cells/Progenitors by Hoechst Dye Efflux Assay
Bhattacharya, S., Jackson, J. D., Das, A. V., Thoreson, W. B., KUSZYNSKI, C. A., James, J., Joshi, S., & Ahmad, I. (2003) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.02-0899 · Cited by 98 · see citing works
Self-citation[56] Lineage analysis using retrovirus vectors
Cepko, C. L., Ryder, E. F., Austin, C. P., Walsh, C. A., & Fekete, D. M. (1993) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/0076-6879(93)25059-b · Cited by 95 · see citing works
Characterization of neurosphere cell phenotypes by flow cytometry
Hulspas, R., & Quesenberry, P. J. (2000) · Cytometry · doi:10.1002/1097-0320(20000701)40:3 · Cited by 93 · see citing works
The Notch Ligand Jagged-1 Is Able to Induce Maturation of Monocyte-Derived Human Dendritic Cells
Weijzen, S., Velders, M. P., Elmishad, A. G., Bacon, P. E., Panella, J. R., Nickoloff, B. J., Miele, L., & Kast, W. M. (2002) · The Journal of Immunology · doi:10.4049/jimmunol.169.8.4273 · Cited by 93 · see citing works
Maintenance of retinal stem cells byAbcg2is regulated by notch signaling
Bhattacharya, S., Das, A. V., Mallya, K. B., & Ahmad, I. (2007) · Journal of Cell Science · doi:10.1242/jcs.008417 · Cited by 83 · see citing works
Self-citationStrategies for retinal repair: cell replacement and regeneration
Lamba, D. A., Karl, M., & Reh, T. A. (2009) · Progress in brain research · doi:10.1016/s0079-6123(09)17502-7 · Cited by 81 · see citing works
James, J., Das, A. V., Rahnenführer, J., & Ahmad, I. (2004) · Journal of Neurobiology · doi:10.1002/neu.20064 · Cited by 64 · see citing works
Self-citationGrowth factor‐responsive progenitors in the postnatal mammalian retina
Zhao, X., Das, A. V., Soto‐Leon, F., & Ahmad, I. (2005) · Developmental Dynamics · doi:10.1002/dvdy.20290 · Cited by 55 · see citing works
Self-citationBhattacharya, S., Das, A. V., Mallya, K. B., & Ahmad, I. (2008) · Stem Cells · doi:10.1634/stemcells.2008-0222 · Cited by 45 · see citing works
Self-citationMouthon, M., Fouchet, P., Mathieu, C., Sii-Felice, K., Etienne, O., Lages, C. S., & Boussin, F. D. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2006.04118.x · Cited by 45 · see citing works
Characterization of liver function in transdifferentiated hepatocytes
Burke, Z. D., Shen, C., Ralphs, K. L., & Tosh, D. (2005) · Journal of Cellular Physiology · doi:10.1002/jcp.20438 · Cited by 43 · see citing works
Baf60c is a component of the neural progenitor‐specific BAF complex in developing retina
Lamba, D. A., Hayes, S., Karl, M., & Reh, T. A. (2008) · Developmental Dynamics · doi:10.1002/dvdy.21697 · Cited by 43 · see citing works
Zhao, X., Das, A. V., Bhattacharya, S., Thoreson, W. B., Rodriguez‐Sierra, J. F., Mallya, K. B., & Ahmad, I. (2008) · Stem Cells · doi:10.1634/stemcells.2007-0727 · Cited by 34 · see citing works
Self-citationThe Canonical Wnt Pathway Regulates Retinal Stem Cells/Progenitors in Concert with Notch Signaling
Das, A. V., Bhattacharya, S., Zhao, X., Hegde, G. V., Mallya, K. B., Eudy, J. D., & Ahmad, I. (2008) · Developmental Neuroscience · doi:10.1159/000178017 · Cited by 33 · see citing works
Self-citationIn vitro analysis of promoter activity in Müller cells.
Geller, S. F., Ge, P. S., Visel, M., & Flannery, J. G. (2008) · PubMed Central · Cited by 7 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Müller glial cell reprogramming and retina regeneration
Goldman, D. J. (2014) · Nature reviews. Neuroscience · doi:10.1038/nrn3723 · Cited by 629 · see citing works
The zebrafish as a model for complex tissue regeneration
Gemberling, M. P., Bailey, T. J., Hyde, D. R., & Poss, K. D. (2013) · Trends in Genetics · doi:10.1016/j.tig.2013.07.003 · Cited by 564 · see citing works
Müller glia: Stem cells for generation and regeneration of retinal neurons in teleost fish
Lenkowski, J. R., & Raymond, P. A. (2014) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2013.12.007 · Cited by 322 · see citing works
HB-EGF is Necessary and Sufficient for Müller Glia Dedifferentiation and Retina Regeneration
Wan, J., Ramachandran, R., & Goldman, D. (2012) · Developmental Cell · doi:10.1016/j.devcel.2011.11.020 · Cited by 262 · see citing works
“[PubMed: 16949068] Del Debbio CB, Balasubramanian S, Parameswaran S, Chaudhuri A, Qiu F, Ahmad I. Notch and Wnt signaling mediated rod photoreceptor regeneration by Muller cells in adult mammalian retina.”
BackgroundInfluentialASCL1 reprograms mouse Müller glia into neurogenic retinal progenitors
Pollak, J., Wilken, M. S., Ueki, Y., Cox, K. E., Sullivan, J., Taylor, R. J., Levine, E. M., & Reh, T. A. (2013) · Development · doi:10.1242/dev.091355 · Cited by 243 · see citing works
Age‐Related Macular Degeneration: New Paradigms for Treatment and Management of AMD
Hernández-Zimbrón, L. F., Zamora-Alvarado, R., la Paz, L. D. O.-D., Vélez-Montoya, R., Zenteno, E., Gulías-Cañizo, R., Quiroz–Mercado, H., & González-Salinas, R. (2018) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2018/8374647 · Cited by 239 · see citing works
A comparative view of regenerative neurogenesis in vertebrates
Alunni, A., & Bally‐Cuif, L. (2016) · Development · doi:10.1242/dev.122796 · Cited by 189 · see citing works
Reprogramming Müller Glia to Regenerate Retinal Neurons
Lahne, M., Nagashima, M., Hyde, D. R., & Hitchcock, P. F. (2020) · Annual Review of Vision Science · doi:10.1146/annurev-vision-121219-081808 · Cited by 159 · see citing works
β-catenin/Wnt signaling controls progenitor fate in the developing and regenerating zebrafish retina
Meyers, J. R., Hu, L., Moses, A., Kaboli, K., Papandrea, A., & Raymond, P. A. (2012) · Neural Development · doi:10.1186/1749-8104-7-30 · Cited by 144 · see citing works
Cell-Based Therapy for Degenerative Retinal Disease
Zarbin, M. A. (2016) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2015.12.007 · Cited by 153 · see citing works
Conner, C., Ackerman, K. M., Lahne, M., Hobgood, J. S., & Hyde, D. R. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0498-14.2014 · Cited by 146 · see citing works
Hamon, A., Roger, J. E., Yang, X.-J., & Perron, M. (2015) · Developmental Dynamics · doi:10.1002/dvdy.24375 · Cited by 139 · see citing works
Cellular strategies for retinal repair by photoreceptor replacement
Jayakody, S. A., Gonzalez-Cordero, A., Ali, R. R., & Pearson, R. A. (2015) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2015.01.003 · Cited by 126 · see citing works
SOX2 maintains the quiescent progenitor cell state of postnatal retinal Müller glia
Surzenko, N., Crowl, T., Bachleda, A., Langer, L., & Pevny, L. (2013) · Development · doi:10.1242/dev.071878 · Cited by 118 · see citing works
Cell-Based Therapy for Degenerative Retinal Disease
Zarbin, M. A. (2019) · Stem cell biology and regenerative medicine · doi:10.1007/978-3-030-05222-5 · Cited by 106 · see citing works
Jayaram, H., Jones, M. F., Eastlake, K., Cottrill, P. B., Becker, S., Wiseman, J., Khaw, P. T., & Limb, G. A. (2014) · Stem Cells Translational Medicine · doi:10.5966/sctm.2013-0112 · Cited by 101 · see citing works
Miyake, M., Yamashiro, K., Tabara, Y., Suda, K., Morooka, S., Nakanishi, H., Khor, C. C., Chen, P., Qiao, F., Nakata, I., et al. (2015) · Nature Communications · doi:10.1038/ncomms7689 · Cited by 93 · see citing works
Wnt Signaling Promotes Müller Cell Proliferation and Survival after Injury
Liu, B., Hunter, D. J., Rooker, S. M., Chan, A. Y., Paulus, Y. M., Leucht, P., Nusse, Y. M., Nomoto, H., & Helms, J. A. (2012) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.12-10774 · Cited by 92 · see citing works
Müller cells as a target for retinal therapy
Devoldere, J., Peynshaert, K., Smedt, S. C. D., & Remaut, K. (2019) · Drug Discovery Today · doi:10.1016/j.drudis.2019.01.023 · Cited by 88 · see citing works
Müller Glia-Mediated Retinal Regeneration
Gao, H., Luodan, A., Huang, X., Chen, X., & Xu, H. (2021) · Molecular Neurobiology · doi:10.1007/s12035-020-02274-w · Cited by 83 · see citing works
Joly, S., Pernet, V., Samardzija, M., & Grimm, C. (2011) · Glia · doi:10.1002/glia.21174 · Cited by 81 · see citing works
Age-dependent Müller glia neurogenic competence in the mouse retina
Loeffler, K., Schäfer, P., Völkner, M., Holdt, T., & Karl, M. (2015) · Glia · doi:10.1002/glia.22846 · Cited by 78 · see citing works
Prospects for the application of Müller glia and their derivatives in retinal regenerative therapies
Eastlake, K., Lamb, W. D. B., Luis, J., Khaw, P. T., Jayaram, H., & Limb, G. A. (2021) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2021.100970 · Cited by 72 · see citing works
Concise Review: Toward Stem Cell-Based Therapies for Retinal Neurodegenerative Diseases
Bull, N. D., & Martin, K. R. G. (2011) · Stem Cells · doi:10.1002/stem.676 · Cited by 69 · see citing works
Retinal regeneration in birds and mice
Wilken, M. S., & Reh, T. A. (2016) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2016.05.028 · Cited by 60 · see citing works
The Regulation of Notch Signaling in Retinal Development and Regeneration
Mills, E. A., & Goldman, D. J. (2017) · Current Pathobiology Reports · doi:10.1007/s40139-017-0153-7 · Cited by 57 · see citing works
Müller Glia: A Promising Target for Therapeutic Regeneration
Ahmad, I., Debbio, C. B. D., Das, A. V., & Parameswaran, S. (2011) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.11-7308 · Cited by 57 · see citing works
Self-citationRetinal regeneration requires dynamic Notch signaling
Hyde, D. R., Campbell, L. J., Levendusky, J., & Steines, S. (2021) · Neural Regeneration Research · doi:10.4103/1673-5374.327326 · Cited by 49 · see citing works
Insights on the Regeneration Potential of Müller Glia in the Mammalian Retina
Salman, A. M., McClements, M. E., & MacLaren, R. E. (2021) · Cells · doi:10.3390/cells10081957 · Cited by 45 · see citing works
Proliferation Potential of Müller Glia after Retinal Damage Varies between Mouse Strains
Suga, A., Sadamoto, K., Fujii, M., Mandai, M., & Takahashi, M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0094556 · Cited by 45 · see citing works
Multiple intrinsic factors act in concert with Lhx2 to direct retinal gliogenesis
de Melo, J., Clark, B. S., & Blackshaw, S. (2016) · Scientific Reports · doi:10.1038/srep32757 · Cited by 42 · see citing works
Ferretti, P. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07833.x · Cited by 42 · see citing works
Lecca, D., Ceruti, S., Fumagalli, M., & Abbracchio, M. P. (2012) · Purinergic Signalling · doi:10.1007/s11302-012-9310-y · Cited by 42 · see citing works
Beyond Genetics: The Role of Metabolism in Photoreceptor Survival, Development and Repair
Hanna, J., David, L. A., Touahri, Y., Fleming, T., Screaton, R. A., & Schuurmans, C. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.887764 · Cited by 43 · see citing works
Rat BMSCs initiate retinal endogenous repair through NGF/TrkA signaling
Jian, Q., Li, Y., & Yin, Z. Q. (2015) · Experimental Eye Research · doi:10.1016/j.exer.2015.01.008 · Cited by 40 · see citing works
Recapitulating developmental mechanisms for retinal regeneration
Ahmad, I., Teotia, P., Erickson, H. E., & Xia, X. (2019) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2019.100824 · Cited by 40 · see citing works
Self-citationHmga2 regulates self-renewal of retinal progenitors
Parameswaran, S., Xia, X., Hegde, G., & Ahmad, I. (2014) · Development · doi:10.1242/dev.107326 · Cited by 40 · see citing works
Self-citationGene-agnostic therapeutic approaches for inherited retinal degenerations
John, M. C., Quinn, J., Hu, M. L., Cehajic‐Kapetanovic, J., & Xue, K. (2023) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.1068185 · Cited by 39 · see citing works
Han, J. W., Lyu, J., Park, Y. J., Jang, S. Y., & Park, T. K. (2015) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.15-18359 · Cited by 39 · see citing works
Patel, A. K., Surapaneni, K. R., Yi, H., Nakamura, R. E. I., Karli, S. Z., Syeda, S., Lee, T., & Hackam, A. S. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.11.015 · Cited by 37 · see citing works
Yu, H., Enayati, S., Chang, K., Cho, K., Lee, S. W., Talib, M., Enayati, K. Z., Xie, J., Achour, H., Fried, S. I., et al. (2020) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.61.4.5 · Cited by 36 · see citing works
TNFα activates MAPK and Jak-Stat pathways to promote mouse Müller cell proliferation.
Niu, L., Fang, Y., Yao, X., Zhang, Y., Wu, J., Chen, D. F., & Sun, X. (2021) · Experimental Eye Research · doi:10.1016/j.exer.2020.108353 · Cited by 32 · see citing works
Debbio, C. B. D., Xu, P., Xiong, H., & Ahmad, I. (2013) · BMC Neuroscience · doi:10.1186/1471-2202-14-130 · Cited by 31 · see citing works
Self-citationMobilizing endogenous stem cells for retinal repair
Yu, H., Vu, T. H. K., Cho, K., Guo, C., & Chen, D. F. (2013) · Translational research · doi:10.1016/j.trsl.2013.11.011 · Cited by 31 · see citing works
Angbohang, A., Wu, N., Charalambous, T., Eastlake, K., Lei, Y., Kim, Y. S., Sun, X., & Limb, G. A. (2015) · Stem Cells and Development · doi:10.1089/scd.2015.0262 · Cited by 29 · see citing works
Besser, M., Jagatheaswaran, M., Reinhard, J., Schaffelke, P., & Faissner, A. (2012) · Developmental Biology · doi:10.1016/j.ydbio.2012.05.020 · Cited by 28 · see citing works
Debbio, C. B. D., Mir, Q. A., Parameswaran, S., Mathews, S., Xia, X., Zheng, L. H., Neville, A. J., & Ahmad, I. (2016) · PLoS ONE · doi:10.1371/journal.pone.0152025 · Cited by 28 · see citing works
Self-citationDNA damage response in proliferating Müller glia in the mammalian retina
Nomura-Komoike, K., Saitoh, F., Komoike, Y., & Fujieda, H. (2016) · Investigative Opthalmology & Visual Science · doi:10.1167/iovs.15-18101 · Cited by 25 · see citing works
Zhang, J., Yan, R., Tang, Y.-S., Guo, Y., Chang, Y., Li, J., Wang, Y., & Zhang, J.-Z. (2017) · International Journal of Immunopathology and Pharmacology · doi:10.1177/0394632017740061 · Cited by 25 · see citing works
Spectral domain optical coherence tomography imaging of mucopolysaccharidoses I, II, and VI A
Seok, S., Lyu, I. J., Park, K. A., & Oh, S. Y. (2015) · Graefe s Archive for Clinical and Experimental Ophthalmology · doi:10.1007/s00417-015-2953-y · Cited by 25 · see citing works
Müller cells trophism and pathology as the next therapeutic targets for retinal diseases
Arrigo, A., Cremona, O., Aragona, E., Casoni, F., Consalez, G., Dogru, R. M., Hauck, S. M., Antropoli, A., Bianco, L., Parodi, M. B., et al. (2025) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2025.101357 · Cited by 25 · see citing works
Jian, Q., Tao, Z., Li, Y., & Yin, Z. Q. (2015) · Vision Research · doi:10.1016/j.visres.2015.01.030 · Cited by 24 · see citing works
Müller glia express rhodopsin in a mouse model of inherited retinal degeneration
Goel, M., & Dhingra, N. K. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.08.066 · Cited by 23 · see citing works
De novo neurogenesis by targeted expression of Atoh7 to Müller glia cells
Lust, K., Sinn, R., Saturnino, A. P., Centanin, L., & Wittbrodt, J. (2016) · Development · doi:10.1242/dev.135905 · Cited by 21 · see citing works
Gu, D., Wang, S., Zhang, S., Zhang, P., & Zhou, G. (2017) · Molecular Medicine Reports · doi:10.3892/mmr.2017.7652 · Cited by 21 · see citing works
Unlocking the Neurogenic Potential of Mammalian Müller Glia
Xia, X., & Ahmad, I. (2016) · International Journal of Stem Cells · doi:10.15283/ijsc16020 · Cited by 20 · see citing works
Self-citationAdvances in the study of Müller glia reprogramming in mammals
Guo, Y.-M., Jiang, X., Min, J., Huang, J., Huang, X., & Lu, Y. (2023) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2023.1305896 · Cited by 18 · see citing works
Zhu, L., Shen, W., Zhang, T., Wang, Y., Bahrami, B., Zhou, F., & Gillies, M. C. (2018) · Experimental Eye Research · doi:10.1016/j.exer.2018.06.016 · Cited by 18 · see citing works
Prospective purification and characterization of Müller glia in the mouse retina regeneration assay
Schäfer, P., & Karl, M. (2017) · Glia · doi:10.1002/glia.23130 · Cited by 17 · see citing works
Emerging pharmacological approaches to promote neurogenesis from endogenous glial cells
Boda, E., Nato, G., & Buffo, A. (2017) · Biochemical Pharmacology · doi:10.1016/j.bcp.2017.06.129 · Cited by 16 · see citing works
Grigoryan, E. N. (2018) · Biochemistry (Moscow) · doi:10.1134/s0006297918110032 · Cited by 14 · see citing works
Cell-Based Therapies for Ocular Disease
Eveleth, D. D. (2013) · Journal of Ocular Pharmacology and Therapeutics · doi:10.1089/jop.2013.0028 · Cited by 13 · see citing works
Sherpa, R. D., & Hui, S. P. (2021) · Animal Models and Experimental Medicine · doi:10.1002/ame2.12177 · Cited by 12 · see citing works
Grigoryan, E. N. (2020) · Biomedicines · doi:10.3390/biomedicines8070208 · Cited by 12 · see citing works
Cell Sources for Retinal Regeneration: Implication for Data Translation in Biomedicine of the Eye
Grigoryan, E. N. (2022) · Cells · doi:10.3390/cells11233755 · Cited by 12 · see citing works
Endogenous Cell Sources for Eye Retina Regeneration in Vertebrate Animals and Humans
Grigoryan, E. N. (2018) · Russian Journal of Developmental Biology · doi:10.1134/s106236041901003x · Cited by 10 · see citing works
Challenges in Retinal Circuit Regeneration
Osakada, F., & Takahashi, M. (2015) · Biological and Pharmaceutical Bulletin · doi:10.1248/bpb.b14-00771 · Cited by 9 · see citing works
Wood, E. H., Korot, E., Storey, P. P., Muscat, S. P., Williams, G. A., & Drenser, K. A. (2020) · Current Opinion in Ophthalmology · doi:10.1097/icu.0000000000000656 · Cited by 9 · see citing works
Zhang, J., Ma, Y., Li, J., Wang, Y., & Zhang, J.-Z. (2020) · Pathology - Research and Practice · doi:10.1016/j.prp.2020.152953 · Cited by 9 · see citing works
Zarbin, M. A. (2012) · Drug Discovery Today Therapeutic Strategies · doi:10.1016/j.ddstr.2012.08.001 · Cited by 8 · see citing works
Interneuron regeneration after ouabain treatment in the adult mammalian retina
Li, Y., & Zhou, G. (2015) · Neuroreport · doi:10.1097/wnr.0000000000000414 · Cited by 6 · see citing works
The Regenerative Potential of the Vertebrate Retina: Lessons from the Zebrafish
Jeremy, N., Currie, P. D., & Jusuf, P. R. (2014) · Stem cell biology and regenerative medicine · doi:10.1007/978-1-4939-0787-8_3 · Cited by 6 · see citing works
Wang, Y., Li, J., Zhang, J., Pang, B., Zhao, Q., Chang, Y., & Jiang, Y. (2017) · Neural Regeneration Research · doi:10.4103/1673-5374.220779 · Cited by 6 · see citing works
Gullapalli, V. K., Khodair, M. A., Wang, H., Sugino, I. K., Madreperla, S. A., & Zarbin, M. A. (2012) · Elsevier eBooks · doi:10.1016/b978-1-4557-0737-9.00125-9 · Cited by 6 · see citing works
Notch Is Required for Neural Progenitor Proliferation During Embryonic Eye Regrowth
Guerin, D. J., Gutierrez, B., Zhang, B., & Tseng, K. A.-S. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26062637 · Cited by 4 · see citing works
Debbio, C. B. D., Parameswaran, S., Das, A. V., & Ahmad, I. (2012) · Springer eBooks · doi:10.1007/978-1-4614-3801-4_9 · Cited by 5 · see citing works
Self-citationCell-based therapy for retinal degenerative disease
(2016) · The Indian Journal of Medical Research · doi:10.4103/0971-5916.178628 · Cited by 3 · see citing works
Photoreceptor Transplantation and Regeneration
Marigo, V., & Casarosa, S. (2014) · Springer eBooks · doi:10.1007/978-4-431-54880-5_12 · Cited by 2 · see citing works
Plagl1 regulates the retinal progenitor cell to Müller glial cell transition
Touahri, Y., Pak, A., David, L. A., Hanna, J., Liu, H., Xiao, Y., Belfiore, L., Ilnytskyy, Y., van Oosten, E., Tachibana, N., et al. (2026) · PLoS Genetics · doi:10.1371/journal.pgen.1012020 · Cited by 1 · see citing works
Stem Cells in the Developing and Adult Nervous System
Osakada, F., & Takahashi, M. (2010) · Springer eBooks · doi:10.1007/978-90-481-9075-1_5 · Cited by 1 · see citing works
Sobacı, G., & Gökçe, G. (2013) · Niche Journal · doi:10.5152/niche.2012.08 · Cited by 1 · see citing works
Mobilizing Endogenous Stem Cells for Retinal Repair
Yu, H., Talib, M., Vu, T. H. K., Cho, K., Guo, C., & Chen, D. F. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-800548-4.00020-6 · Cited by 1 · see citing works
Touahri, Y., David, L. A., Ilnytskyy, Y., van Oosten, E., Hanna, J., Tachibana, N., Adnani, L., Zhao, J., Hoffman, M., Dixit, R., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.04.12.439550 · Cited by 1 · see citing works
Stem Cells and Ocular Disorders: Basic Science to Clinical Applications
(2012) · BENTHAM SCIENCE PUBLISHERS eBooks · doi:10.2174/978160805289911201010168
Baker, R., & Sharp, M. (2012)
Retinal Repair Using Stem Cells
Gutierrez, M. A., & Lamba, D. A. (2015) · Springer eBooks · doi:10.1007/978-3-7091-1232-8_15
Regenerative Therapies for Retinopathy
Periasamy, R., & Gangaraju, R. (2016) · Springer eBooks · doi:10.1007/978-3-319-28293-0_9
Johnson, T. V., & Martin, K. R. G. (2014) · Elsevier eBooks · doi:10.1016/b978-0-7020-5193-7.00063-7
Hope or Hype: Stem Cells as Therapeutics in Retinal Degenerative Diseases
Parameswaran, S. (2018) · Springer eBooks · doi:10.1007/978-981-13-0481-1_8
Self-citationStem Cells in the Developing and Adult Nervous System
Osakada, F., & Takahashi, M. (2016) · Springer eBooks · doi:10.1007/978-3-319-27583-3_4
Stem Cells in the Developing and Adult Nervous System
Osakada, F., & Takahashi, M. (2013) · Springer eBooks · doi:10.1007/978-94-007-5690-8_5
Cell-Based Therapy for Retinal Degenerative Disease
Zarbin, M. A. (2018) · Springer eBooks · doi:10.1007/978-3-319-90695-9_5
Cellular and molecular mechanisms of retinal regeneration in the axolotl salamander
Yandulskaya, A. S. (2022) · doi:10.17760/d20439213
A Literary Pediatric Retina Fellowship With Michael T. Trese, MD
Wood, E. H., Moshfeghi, D. M., Capone, A., Williams, G. A., Blumenkranz, M. S., Sieving, P. A., Harper, C. A., Hartnett, M. E., & Drenser, K. A. (2023) · Ophthalmic surgery, lasers & imaging retina · doi:10.3928/23258160-20231020-01
Retinal microstructual and microvascular changes in mucopolysaccharidoses
Wipprecht, L., Borchers, A. J., Stingl, J. V., Schmitz, L. S., von Plettenberg, K., Hennermann, J. B., Hopf, S., Pitz, S., & Matlach, J. (2025) · Graefe s Archive for Clinical and Experimental Ophthalmology · doi:10.1007/s00417-025-06954-y
- Authors
- Del Debbio, C. B., Balasubramanian, S., Parameswaran, S., Chaudhuri, A., Qiu, F., & Ahmad, I.
- Affiliations
- University of Nebraska Medical Center (US)
- Corresponding author
- Ahmad, Iqbal
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2010-08-26
- Volume
- 5
- Issue
- 8
- Pages
- e12425
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC2928741
- OpenAlex
- W2075249408
- Cited by
- 103
- References
- 58
- Citations by year
- 2026: 3 · 2025: 3 · 2023: 3 · 2022: 3 · 2021: 6 · 2020: 7 · 2019: 4 · 2018: 6 · 2017: 6 · 2016: 11 · 2015: 13 · 2014: 10 · 2013: 10 · 2012: 12
- FWCI
- 3.65
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Funders
- U.S. Department of Health and Human Services
- Research to Prevent Blindness
- Lincy Foundation
- Nebraska Department of Health and Human Services
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Retinal Development and Disorders
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Health Sciences › Medicine › Ophthalmology › Retinal Diseases and Treatments
- Keywords
- Müller cells, Notch signaling, Wnt signaling, retinal stem cells, light perception
- MeSH terms
- Animals, Mammals, Mice, Inbred C57BL, Regeneration, Retina, Vision, Ocular, Retinal Rod Photoreceptor Cells, Wnt Proteins, Mice, Rats, Receptors, Notch
About these checks
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.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
