Show simple item record

The MicroRNA, miR‐18a, Regulates NeuroD and Photoreceptor Differentiation in the Retina of Zebrafish

dc.contributor.authorTaylor, Scott M.
dc.contributor.authorGiuffre, Emily
dc.contributor.authorMoseley, Patience
dc.contributor.authorHitchcock, Peter F.
dc.date.accessioned2019-02-12T20:24:35Z
dc.date.available2020-04-01T15:06:24Zen
dc.date.issued2019-02
dc.identifier.citationTaylor, Scott M.; Giuffre, Emily; Moseley, Patience; Hitchcock, Peter F. (2019). "The MicroRNA, miR‐18a, Regulates NeuroD and Photoreceptor Differentiation in the Retina of Zebrafish." Developmental Neurobiology 79(2): 202-219.
dc.identifier.issn1932-8451
dc.identifier.issn1932-846X
dc.identifier.urihttps://hdl.handle.net/2027.42/147840
dc.description.abstractDuring embryonic retinal development, six types of retinal neurons are generated from multipotent progenitors in a strict spatiotemporal pattern. This pattern requires cell cycle exit (i.e. neurogenesis) and differentiation to be precisely regulated in a lineage‐specific manner. In zebrafish, the bHLH transcription factor NeuroD governs photoreceptor genesis through Notch signaling but also governs photoreceptor differentiation though distinct mechanisms that are currently unknown. Also unknown are the mechanisms that regulate NeuroD and the spatiotemporal pattern of photoreceptor development. Members of the miR‐17‐92 microRNA cluster regulate CNS neurogenesis, and a member of this cluster, miR‐18a, is predicted to target neuroD mRNA. The purpose of this study was to determine if, in the developing zebrafish retina, miR‐18a regulates NeuroD and if it plays a role in photoreceptor development. Quantitative RT‐PCR showed that, of the three miR‐18 family members (miR‐18a, b, and c), miR‐18a expression most closely parallels neuroD expression. Morpholino oligonucleotides and CRISPR/Cas9 gene editing were used for miR‐18a loss‐of‐function (LOF) and both resulted in larvae with more mature photoreceptors at 70 hpf without affecting cell proliferation. Western blot showed that miR‐18a LOF increases NeuroD protein levels and in vitro dual luciferase assay showed that miR‐18a directly interacts with the 3′ UTR of neuroD. Finally, tgif1 mutants have increased miR‐18a expression, less NeuroD protein and fewer mature photoreceptors, and the photoreceptor deficiency is rescued by miR‐18a knockdown. Together, these results show that, independent of neurogenesis, miR‐18a regulates the timing of photoreceptor differentiation and indicate that this occurs through post‐transcriptional regulation of NeuroD.
dc.publisherHumana Press
dc.publisherWiley Periodicals, Inc.
dc.subject.otherretinal development
dc.subject.otherpost‐transcriptional
dc.subject.othermiRNA
dc.subject.otherneurogenesis
dc.subject.otherbHLH
dc.subject.otherphotoreceptors
dc.titleThe MicroRNA, miR‐18a, Regulates NeuroD and Photoreceptor Differentiation in the Retina of Zebrafish
dc.typeArticleen_US
dc.rights.robotsIndexNoFollow
dc.subject.hlbsecondlevelNeurosciences
dc.subject.hlbtoplevelHealth Sciences
dc.description.peerreviewedPeer Reviewed
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/147840/1/dneu22666.pdf
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/147840/2/dneu22666_am.pdf
dc.identifier.doi10.1002/dneu.22666
dc.identifier.sourceDevelopmental Neurobiology
dc.identifier.citedreferencePollak, J., Wilken, M.S., Ueki, Y., Cox, K.E., Sullivan, J.M., Taylor, R.J. et al. ( 2013 ) ASCL1 reprograms mouse Muller glia into neurogenic retinal progenitors. Development (Cambridge, England), 140 ( 12 ), 2619 – 2631. Available at: https://doi.org/10.1242/dev.091355.
dc.identifier.citedreferenceParchem, R.J., Moore, N., Fish, J.L., Parchem, J.G., Braga, T.T., Shenoy, A. et al. ( 2015 ) miR‐302 Is required for timing of neural differentiation, neural tube closure, and embryonic viability. Cell Reports, 12 ( 5 ), 760 – 773. Available at: https://doi.org/10.1016/j.celrep.2015.06.074.
dc.identifier.citedreferencePeter, M.E. ( 2010 ) Targeting of mRNAs by multiple miRNAs: the next step. Oncogene, 29 ( 15 ), 2161 – 2164. Available at: https://doi.org/10.1038/onc.2010.59.
dc.identifier.citedreferencePetri, R., Malmevik, J., Fasching, L., Åkerblom, M. and Jakobsson, J. ( 2014 ) miRNAs in brain development. Experimental Cell Research, 321 ( 1 ), 84 – 89. Available at: https://doi.org/10.1016/j.yexcr.2013.09.022.
dc.identifier.citedreferencePham, J.T. and Gallicano, G.I. ( 2012 ) Specification of neural cell fate and regulation of neural stem cell proliferation by microRNAs. American Journal of Stem Cells, 1 ( 3 ), 182 – 195. papers3://publication/uuid/2D0AFD65-6542-4CF3-A25A-AE617D04EA3C.
dc.identifier.citedreferencePowrózek, T., Mlak, R., Dziedzic, M., Małecka‐Massalska, T. and Sagan, D. ( 2018 ) Investigation of relationship between precursor of miRNA‐944 and its mature form in lung squamous‐cell carcinoma—the diagnostic value. Pathology ‐ Research and Practice, 214 ( 3 ), 368 – 373. Available at: https://doi.org/10.1016/j.prp.2018.01.002.
dc.identifier.citedreferenceRaymond, P.A. and Barthel, L.K. ( 2004 ) A moving wave patterns the cone photoreceptor mosaic array in the zebrafish retina. The International Journal of Developmental Biology, 48 ( 8–9 ), 935 – 945. Available at: https://doi.org/10.1387/ijdb.041873pr.
dc.identifier.citedreferenceRaymond, P.A., Colvin, S.M., Jabeen, Z., Nagashima, M., Barthel, L.K., Hadidjojo, J. et al. ( 2014 ) Patterning the cone mosaic array in zebrafish retina requires specification of ultraviolet‐sensitive cones. PLoS ONE, 9 ( 1 ), e85325. Available at: https://doi.org/10.1371/journal.pone.0085325.
dc.identifier.citedreferenceSchmitt, E.A. and Dowling, J.E. ( 1999 ) Early retinal development in the zebrafish, Danio rerio: light and electron microscopic analyses. The Journal of Comparative Neurology, 404 ( 4 ), 515 – 536.
dc.identifier.citedreferenceShah, M.Y., Ferrajoli, A., Sood, A.K., Lopez‐Berestein, G. and Calin, G.A. ( 2016 ) microRNA therapeutics in cancer—an emerging concept. EBioMedicine, 12, 34 – 42. Available at: https://doi.org/10.1016/j.ebiom.2016.09.017.
dc.identifier.citedreferenceShi, Y., Zhao, X., Hsieh, J., Wichterle, H., Impey, S., Banerjee, S. et al. ( 2010 ) MicroRNA regulation of neural stem cells and neurogenesis. Journal of Neuroscience, 30 ( 45 ), 14931 – 14936. Available at: https://doi.org/10.1523/JNEUROSCI.4280-10.2010.
dc.identifier.citedreferenceStenkamp, D.L. ( 2007 ) Neurogenesis in the fish retina. International Review of Cytology, 259, 173 – 224. Available at: https://doi.org/10.1016/S0074-7696(06)59005-9.
dc.identifier.citedreferenceStenkamp, D.L. ( 2015 ) Development of the vertebrate eye and retina. Progress in Molecular Biology and Translational Science, 134, 397 – 414. Available at: https://doi.org/10.1016/bs.pmbts.2015.06.006.
dc.identifier.citedreferenceSundermeier, T.R. and Palczewski, K. ( 2016 ) The impact of microRNA gene regulation on the survival and function of mature cell types in the eye. FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology, 30 ( 1 ), 23 – 33. Available at: https://doi.org/10.1096/fj.15-279745.
dc.identifier.citedreferenceTaylor, S.M., Alvarez‐Delfin, K., Saade, C., Thomas, J.L., Thummel, R., Fadool, J.M. et al. ( 2015 ) The bHLH transcription factor NeuroD governs photoreceptor genesis and regeneration through Delta‐Notch signaling. Investigative Ophthalmology & Visual Science, 56 ( 12 ), 7496 – 7515. Available at: https://doi.org/10.1167/iovs.15-17616.
dc.identifier.citedreferenceUeki, Y. and Reh, T.A. ( 2013 ) EGF stimulates müller glial proliferation via a BMP‐dependent mechanism. Glia, 61 ( 5 ), 778 – 789. Available at: https://doi.org/10.1002/glia.22472.
dc.identifier.citedreferenceValencia‐Sanchez, M.A., Liu, J., Hannon, G.J. and Parker, R. ( 2006 ) Control of translation and mRNA degradation by miRNAs and siRNAs. Genes & Development, 20 ( 5 ), 515 – 524. Available at: https://doi.org/10.1101/gad.1399806.
dc.identifier.citedreferenceVentura, A., Young, A.G., Winslow, M.M., Lintault, L., Meissner, A., Erkeland, S.J. et al. ( 2008 ) Targeted deletion reveals essential and overlapping functions of the miR‐17 through 92 family of miRNA clusters. Cell, 132 ( 5 ), 875 – 886. Available at: https://doi.org/10.1016/j.cell.2008.02.019.
dc.identifier.citedreferenceWallace, V.A. ( 2011 ) Concise review: making a retina—from the building blocks to clinical applications. Stem cells (Dayton, Ohio), 29 ( 3 ), 412 – 417. Available at: https://doi.org/10.1002/stem.602.
dc.identifier.citedreferenceWang, S. and Cepko, C.L. ( 2016 ) Photoreceptor fate determination in the vertebrate retina. Investigative Ophthalmology & Visual Science, 57 ( 5 ), ORSFe1. Available at: https://doi.org/10.1167/iovs.15-17672.
dc.identifier.citedreferenceWinter, J., Jung, S., Keller, S., Gregory, R.I. and Diederichs, S. ( 2009 ) Many roads to maturity: microRNA biogenesis pathways and their regulation. Nature Cell Biology, 11 ( 3 ), 228 – 234. Available at: https://doi.org/10.1038/ncb0309-228.
dc.identifier.citedreferenceZeng, Y., Yi, R. and Cullen, B.R. ( 2003 ) MicroRNAs and small interfering RNAs can inhibit mRNA expression by similar mechanisms. Proceedings of the National Academy of Sciences of the United States of America, 100 ( 17 ), 9779 – 9784. Available at: https://doi.org/10.1073/pnas.1630797100.
dc.identifier.citedreferenceZeng, Y., Yi, R. and Cullen, B.R. ( 2005 ) Recognition and cleavage of primary microRNA precursors by the nuclear processing enzyme Drosha. The EMBO Journal, 24 ( 1 ), 138 – 148. Available at: https://doi.org/10.1038/sj.emboj.7600491.
dc.identifier.citedreferenceZhang, Z.‐W., Zhang, L.‐Q., Ding, L., Wang, F., Sun, Y.‐J., An, Y. et al. ( 2011 ) MicroRNA‐19b downregulates insulin 1 through targeting transcription factor NeuroD1. FEBS Letters, 585 ( 16 ), 2592 – 2598. Available at: https://doi.org/10.1016/j.febslet.2011.06.039.
dc.identifier.citedreferenceZhu, J., Ming, C., Fu, X., Duan, Y., Hoang, D.A., Rutgard, J. et al. ( 2017 ) Gene and mutation independent therapy via CRISPR‐Cas9 mediated cellular reprogramming in rod photoreceptors. Cell Research, 27 ( 6 ), 830 – 833. Available at: https://doi.org/10.1038/cr.2017.57.
dc.identifier.citedreferenceAkagi, T., Inoue, T., Miyoshi, G., Bessho, Y., Takahashi, M., Lee, J.E. et al. ( 2004 ) Requirement of multiple basic helix‐loop‐helix genes for retinal neuronal subtype specification. The Journal of Biological Chemistry, 279 ( 27 ), 28492 – 28498. Available at: https://doi.org/10.1074/jbc.M400871200.
dc.identifier.citedreferenceAllison, W.T., Barthel, L.K., Skebo, K.M., Takechi, M., Kawamura, S. and Raymond, P.A. ( 2010 ) Ontogeny of cone photoreceptor mosaics in zebrafish. The Journal of Comparative Neurology, 518 ( 20 ), 4182 – 4195. Available at: https://doi.org/10.1002/cne.22447.
dc.identifier.citedreferenceAndreeva, K. and Cooper, N.G.F. ( 2014 ) MicroRNAs in the neural retina. International Journal of Genomics, 2014 ( 10 ), 165897 – 165814. Available at: https://doi.org/10.1155/2014/165897.
dc.identifier.citedreferenceBaker, N.E. and Brown, N.L. ( 2018 ) All in the family: proneural bHLH genes and neuronal diversity. Development (Cambridge, England), 145 ( 9 ), dev159426 – 159429. Available at: https://doi.org/10.1242/dev.159426.
dc.identifier.citedreferenceBao, J., Li, D., Wang, L., Wu, J., Hu, Y., Wang, Z. et al. ( 2012 ) MicroRNA‐449 and microRNA‐34b/c function redundantly in murine testes by targeting E2F transcription factor‐retinoblastoma protein (E2F‐pRb) pathway. The Journal of Biological Chemistry, 287 ( 26 ), 21686 – 21698. Available at: https://doi.org/10.1074/jbc.M111.328054.
dc.identifier.citedreferenceBao, J., Vitting‐Seerup, K., Waage, J., Tang, C., Ge, Y., Porse, B.T. et al. ( 2016 ) UPF2‐dependent nonsense‐mediated mRNA decay pathway is essential for spermatogenesis by selectively eliminating longer 3’UTR transcripts. PLoS Genetics, 12 ( 5 ), e1005863. Available at: https://doi.org/10.1371/journal.pgen.1005863.
dc.identifier.citedreferenceBartel, D.P. ( 2004 ) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 116 ( 2 ), 281 – 297. Available at: https://doi.org/10.1016/S0092-8674(04)00045-5.
dc.identifier.citedreferenceBarthel, L.K. and Raymond, P.A. ( 1993 ) Subcellular localization of α‐tubulin and opsin mRNA in the goldfish retina using digoxigenin‐labeled cRNA probes detected by alkaline phosphatase and HRP histochemistry. Journal of Neuroscience Methods, 50 ( 2 ), 145 – 152. Available at: https://doi.org/10.1016/0165-0270(93)90002-9.
dc.identifier.citedreferenceBassett, E.A. and Wallace, V.A. ( 2012 ) Cell fate determination in the vertebrate retina. Trends in Neurosciences, 35 ( 9 ), 565 – 573. Available at: https://doi.org/10.1016/j.tins.2012.05.004.
dc.identifier.citedreferencevan den Berg, A., Mols, J. and Han, J. ( 2008 ) RISC‐target interaction: cleavage and translational suppression. Biochimica Et Biophysica Acta, 1779 ( 11 ), 668 – 677. Available at: https://doi.org/10.1016/j.bbagrm.2008.07.005.
dc.identifier.citedreferenceBian, S., Hong, J., Li, Q., Schebelle, L., Pollock, A., Knauss, J.L. et al. ( 2013 ) MicroRNA cluster miR‐17‐92 regulates neural stem cell expansion and transition to intermediate progenitors in the developing mouse neocortex. Cell Reports, 3 ( 5 ), 1398 – 1406. Available at: https://doi.org/10.1016/j.celrep.2013.03.037.
dc.identifier.citedreferenceBroughton, J.P., Lovci, M.T., Huang, J.L., Yeo, G.W. and Pasquinelli, A.E. ( 2016 ) Pairing beyond the seed supports microRNA targeting specificity. Molecular Cell, 64 ( 2 ), 320 – 333. Available at: https://doi.org/10.1016/j.molcel.2016.09.004.
dc.identifier.citedreferenceBrzezinski, J.A. and Reh, T.A. ( 2015 ) Photoreceptor cell fate specification in vertebrates. Development (Cambridge, England), 142 ( 19 ), 3263 – 3273. Available at: https://doi.org/10.1242/dev.127043.
dc.identifier.citedreferenceBrzezinski, J.A., Kim, E.J., Johnson, J.E. and Reh, T.A. ( 2011 ) Ascl1 expression defines a subpopulation of lineage‐restricted progenitors in the mammalian retina. Development (Cambridge, England), 138 ( 16 ), 3519 – 3531. Available at: https://doi.org/10.1242/dev.064006.
dc.identifier.citedreferenceCentanin, L. and Wittbrodt, J. ( 2014 ) Retinal neurogenesis. Development (Cambridge, England), 141 ( 2 ), 241 – 244. Available at: https://doi.org/10.1242/dev.083642.
dc.identifier.citedreferenceCepko, C. ( 2014 ) Intrinsically different retinal progenitor cells produce specific types of progeny. Nature Chemical Biology, 15 ( 9 ), 615 – 627. Available at: https://doi.org/10.1038/nrn3767.
dc.identifier.citedreferenceChang, H., Yi, B., Ma, R., Zhang, X., Zhao, H. and Xi, Y. ( 2016 ) CRISPR/cas9, a novel genomic tool to knock down microRNA in vitro and in vivo. Scientific Reports, 6 ( 1 ), 22312. Available at: https://doi.org/10.1038/srep22312.
dc.identifier.citedreferenceConte, I., Marco‐Ferreres, R., Beccari, L., Cisneros, E., Ruiz, J.M., Tabanera, N. et al. ( 2010 ) Proper differentiation of photoreceptors and amacrine cells depends on a regulatory loop between NeuroD and Six6. Development (Cambridge, England), 137 ( 14 ), 2307 – 2317. Available at: https://doi.org/10.1242/dev.045294.
dc.identifier.citedreferenceDavid, R. and Wedlich, D. ( 2001 ) PCR‐based RNA probes: a quick and sensitive method to improve whole mount embryo in situ hybridizations. BioTechniques, 30 ( 4 ), 769 – 775. Available at: https://doi.org/10.2144/01304st02.
dc.identifier.citedreferenceDjuranovic, S., Nahvi, A. and Green, R. ( 2012 ) miRNA‐mediated gene silencing by translational repression followed by mRNA deadenylation and decay. Science (New York, NY), 336 ( 6078 ), 237 – 240. Available at: https://doi.org/10.1126/science.1215691.
dc.identifier.citedreferenceDow, L.E., Fisher, J., O’Rourke, K.P., Muley, A., Kastenhuber, E.R., Livshits, G. et al. ( 2015 ) Inducible in vivo genome editing with CRISPR‐Cas9. Nature Biotechnology, 33 ( 4 ), 390 – 394. Available at: https://doi.org/10.1038/nbt.3155.
dc.identifier.citedreferenceFischer, S., Handrick, R., Aschrafi, A. and Otte, K. ( 2015 ) Unveiling the principle of microRNA‐mediated redundancy in cellular pathway regulation. RNA Biology, 12 ( 3 ), 238 – 247. Available at: https://doi.org/10.1080/15476286.2015.1017238.
dc.identifier.citedreferenceFlynt, A.S., Thatcher, E.J., Burkewitz, K., Li, N., Liu, Y. and Patton, J.G. ( 2009 ) miR‐8microRNAs regulate the response to osmotic stress in zebrafish embryos. The Journal of Cell Biology, 185 ( 1 ), 115 – 127. Available at: https://doi.org/10.1083/jcb.200807026.
dc.identifier.citedreferenceFlynt, A.S., Rao, M. and Patton, J.G. ( 2017 ). Blocking zebrafish microRNAs with morpholinos. Methods in Molecular Biology (Clifton, N.J.), 1565, 59 – 78. Available at: https://doi.org/10.1007/978-1-4939-6817-6_6.
dc.identifier.citedreferenceForbes‐Osborne, M.A., Wilson, S.G. and Morris, A.C. ( 2013 ) Insulinoma‐associated 1a (Insm1a) is required for photoreceptor differentiation in the zebrafish retina. Developmental Biology, 380 ( 2 ), 157 – 171. Available at: https://doi.org/10.1016/j.ydbio.2013.05.021.
dc.identifier.citedreferenceFriedman, L.M., Dror, A.A., Mor, E., Tenne, T., Toren, G., Satoh, T. et al. ( 2009 ) MicroRNAs are essential for development and function of inner ear hair cells in vertebrates. Proceedings of the National Academy of Sciences of the United States of America, 106 ( 19 ), 7915 – 7920. Available at: https://doi.org/10.1073/pnas.0812446106.
dc.identifier.citedreferenceGregory‐Evans, C.Y., Wallace, V.A. and Gregory‐Evans, K. ( 2013 ) Gene networks: dissecting pathways in retinal development and disease. Progress in Retinal and Eye Research, 33, 40 – 66. Available at: https://doi.org/10.1016/j.preteyeres.2012.10.003.
dc.identifier.citedreferenceGurtan, A.M. and Sharp, P.A. ( 2013 ) The role of miRNAs in regulating gene expression networks. Journal of Molecular Biology, 425 ( 19 ), 3582 – 3600. Available at: https://doi.org/10.1016/j.jmb.2013.03.007.
dc.identifier.citedreferenceHirosawa, M., Fujita, Y., Parr, C.J.C., Hayashi, K., Kashida, S., Hotta, A. et al. ( 2017 ) Cell‐type‐specific genome editing with a microRNA‐responsive CRISPR–Cas9 switch. Nucleic Acids Research, 45 ( 13 ), e118 – e118. Available at: https://doi.org/10.1093/nar/gkx309.
dc.identifier.citedreferenceHumphreys, D.T., Westman, B.J., Martin, D.I.K. and Preiss, T. ( 2005 ) MicroRNAs control translation initiation by inhibiting eukaryotic initiation factor 4E/cap and poly(A) tail function. Proceedings of the National Academy of Sciences of the United States of America, 102 ( 47 ), 16961 – 16966. Available at: https://doi.org/10.1073/pnas.0506482102.
dc.identifier.citedreferenceHuntzinger, E. and Izaurralde, E. ( 2011 ) Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nature Reviews Genetics, 12 ( 2 ), 99 – 110. Available at: https://doi.org/10.1038/nrg2936.
dc.identifier.citedreferenceHwang, W.Y., Fu, Y., Reyon, D., Maeder, M.L., Tsai, S.Q., Sander, J.D. et al. ( 2013 ) Efficient genome editing in zebrafish using a CRISPR‐Cas system. Nature Biotechnology, 31 ( 3 ), 227 – 229. Available at: https://doi.org/10.1038/nbt.2501.
dc.identifier.citedreferenceIwakawa, H.‐O. and Tomari, Y. ( 2015 ) The Functions of microRNAs: mRNA decay and translational repression. Trends in Cell Biology, 25 ( 11 ), 651 – 665. Available at: https://doi.org/10.1016/j.tcb.2015.07.011.
dc.identifier.citedreferenceJin, Y., Chen, Z., Liu, X. and Zhou, X. ( 2012 ). Evaluating the microRNA targeting sites by luciferase reporter gene assay. In: Ying, S. Y., (Ed.) Methods in Molecular Biology (Clifton, N.J.). Totowa, NJ: Humana Press, Vol. 936, pp. 117 – 127.
dc.identifier.citedreferenceJorstad, N.L., Wilken, M.S., Grimes, W.N., Wohl, S.G., VandenBosch, L.S., Yoshimatsu, T. et al. ( 2017 ) Stimulation of functional neuronal regeneration from Müller glia in adult mice. Nature, 548, 103. Available at: https://doi.org/10.1038/nature23283.
dc.identifier.citedreferenceKhuu, C., Utheim, T.P. and Sehic, A. ( 2016 ) The three paralogous microRNA clusters in development and disease, miR‐17‐92, miR‐106a‐363, and miR‐106b‐25. Scientifica, 2016, 1379643. Available at: https://doi.org/10.1155/2016/1379643.
dc.identifier.citedreferenceLa Torre, A., Georgi, S. and Reh, T.A. ( 2013 ) Conserved microRNA pathway regulates developmental timing of retinal neurogenesis. Proceedings of the National Academy of Sciences of the United States of America, 110 ( 26 ), E2362 – 2370. Available at: https://doi.org/10.1073/pnas.1301837110.
dc.identifier.citedreferenceLenkowski, J.R. and Raymond, P.A. ( 2014 ) Müller glia: stem cells for generation and regeneration of retinal neurons in teleost fish. Progress in Retinal and Eye Research, 40, 94 – 123. Available at: https://doi.org/10.1016/j.preteyeres.2013.12.007.
dc.identifier.citedreferenceLenkowski, J.R., Qin, Z., Sifuentes, C.J., Thummel, R., Soto, C.M., Moens, C.B. et al. ( 2013 ) Retinal regeneration in adult zebrafish requires regulation of TGFβ signaling. Glia, 61 ( 10 ), 1687 – 1697. Available at: https://doi.org/10.1002/glia.22549.
dc.identifier.citedreferenceLuo, J., Uribe, R.A., Hayton, S., Calinescu, A.‐A., Gross, J.M. and Hitchcock, P.F. ( 2012 ) Midkine‐A functions upstream of Id2a to regulate cell cycle kinetics in the developing vertebrate retina. Neural Development, 7 ( 1 ), 33. Available at: https://doi.org/10.1038/nprot.2008.73.
dc.identifier.citedreferenceMadelaine, R., Sloan, S.A., Huber, N., Notwell, J.H., Leung, L.C., Skariah, G. et al. ( 2017 ) MicroRNA‐9 couples brain neurogenesis and angiogenesis. Cell Reports, 20 ( 7 ), 1533 – 1542. Available at: https://doi.org/10.1016/j.celrep.2017.07.051.
dc.identifier.citedreferenceMao, C.‐A., Cho, J.‐H., Wang, J., Gao, Z., Pan, P., Tsai, W.‐W. et al. ( 2013 ) Reprogramming amacrine and photoreceptor progenitors into retinal ganglion cells by replacing Neurod1 with Atoh7. Development (Cambridge, England), 140 ( 3 ), 541 – 551. Available at: https://doi.org/10.1242/dev.085886.
dc.identifier.citedreferenceMattar, P. and Cayouette, M. ( 2015 ) Mechanisms of temporal identity regulation in mouse retinal progenitor cells. Neurogenesis, 2 ( 1 ), e1125409. Available at: https://doi.org/10.1080/23262133.2015.1125409.
dc.identifier.citedreferenceMcLaughlin, J.M., Smith, D.F.Q., Catrina, I.E. and Bratu, D.P. ( 2018 ) P‐bodies and the miRNA pathway regulate translational repression of bicoid mRNA during Drosophila melanogaster oogenesis. bioRxiv, 283630. Available at: https://doi.org/10.1101/283630.
dc.identifier.citedreferenceNasevicius, A. and Ekker, S.C. ( 2000 ) Effective targeted gene ‘knockdown’ in zebrafish. Nature Genetics, 26 ( 2 ), 216 – 220. Available at: https://doi.org/10.1038/79951.
dc.identifier.citedreferenceNepal, C., Coolen, M., Hadzhiev, Y., Cussigh, D., Mydel, P., Steen, V.M. et al. ( 2016 ) Transcriptional, post‐transcriptional and chromatin‐associated regulation of pri‐miRNAs, pre‐miRNAs and moRNAs. Nucleic Acids Research, 44 ( 7 ), 3070 – 3081. Available at: https://doi.org/10.1093/nar/gkv1354.
dc.identifier.citedreferenceOchocinska, M.J. and Hitchcock, P.F. ( 2007 ) Dynamic expression of the basic helix‐loop‐helix transcription factor neuroD in the rod and cone photoreceptor lineages in the retina of the embryonic and larval zebrafish. The Journal of Comparative Neurology, 501 ( 1 ), 1 – 12. Available at: https://doi.org/10.1002/cne.21150.
dc.identifier.citedreferenceOchocinska, M.J. and Hitchcock, P.F. ( 2009 ) NeuroD regulates proliferation of photoreceptor progenitors in the retina of the zebrafish. Mechanisms of Development, 126 ( 3–4 ), 128 – 141. Available at: https://doi.org/10.1016/j.mod.2008.11.009.
dc.identifier.citedreferenceOhana, R., Weiman‐Kelman, B., Raviv, S., Tamm, E.R., Pasmanik‐Chor, M., Rinon, A. et al. ( 2015 ) MicroRNAs are essential for differentiation of the retinal pigmented epithelium and maturation of adjacent photoreceptors. Development (Cambridge, England), 142 ( 14 ), 2487 – 2498. Available at: https://doi.org/10.1242/dev.121533.
dc.identifier.citedreferenceOhsawa, R. and Kageyama, R. ( 2008 ) Regulation of retinal cell fate specification by multiple transcription factors. Brain Research, 1192, 90 – 98. Available at: https://doi.org/10.1016/j.brainres.2007.04.014.
dc.identifier.citedreferenceOlive, V., Minella, A.C. and He, L. ( 2015 ) Outside the coding genome, mammalian microRNAs confer structural and functional complexity. Science Signaling, 8 ( 368 ), re2 – re2. Available at: https://doi.org/10.1126/scisignal.2005813.
dc.owningcollnameInterdisciplinary and Peer-Reviewed


Files in this item

Show simple item record

Remediation of Harmful Language

The University of Michigan Library aims to describe library materials in a way that respects the people and communities who create, use, and are represented in our collections. Report harmful or offensive language in catalog records, finding aids, or elsewhere in our collections anonymously through our metadata feedback form. More information at Remediation of Harmful Language.

Accessibility

If you are unable to use this file in its current format, please select the Contact Us link and we can modify it to make it more accessible to you.