Zebrafish and inherited photoreceptor disease: Models and insights

Abd El-Aziz, 2008, EYS, encoding an ortholog of Drosophila spacemaker, is mutated in autosomal recessive retinitis pigmentosa, Nat. Genet., 40, 1285, 10.1038/ng.241 Ahmed, 2001, Mutations of the protocadherin vene PCDH15 cause Usher syndrome type 1F, Am. J. Hum. Genet., 69, 25, 10.1086/321277 Akahori, 2010, Dominant mutations in RP1L1 are responsible for occult macular dystrophy, Am. J. Hum. Genet., 87, 424, 10.1016/j.ajhg.2010.08.009 Alfano, 2016, EYS is a protein associated with the ciliary axoneme in rods and cones, PLoS One, 11, 1, 10.1371/journal.pone.0166397 Alhasani, 2020, Gypenosides attenuate retinal degeneration in a zebrafish retinitis pigmentosa model, Exp. Eye Res., 201, 10.1016/j.exer.2020.108291 Allison, 2010, Ontogeny of cone photoreceptor mosaics in zebrafish, J. Comp. Neurol., 518, 4182, 10.1002/cne.22447 Allwardt, 2001, Synapse formation is arrested in retinal photoreceptors of the zebrafish nrc mutant, J. Neurosci., 21, 2330, 10.1523/JNEUROSCI.21-07-02330.2001 Anzalone, 2020, Genome editing with CRISPR–Cas nucleases, base editors, transposases and prime editors, Nat. Biotechnol., 38, 824, 10.1038/s41587-020-0561-9 Asai-Coakwell, 2009, Incomplete penetrance and phenotypic variability characterize Gdf6-attributable oculo-skeletal phenotypes, Hum. Mol. Genet., 18, 1110, 10.1093/hmg/ddp008 Asai-Coakwell, 2013, Contribution of growth differentiation factor 6-dependent cell survival to early-onset retinal dystrophies, Hum. Mol. Genet., 22, 1432, 10.1093/hmg/dds560 Bachmann-Gagescu, 2015, KIAA0586 is mutated in Joubert syndrome, Hum. Mutat., 36, 831, 10.1002/humu.22821 Bachmann-Gagescu, 2011, The ciliopathy gene cc2d2a controls zebrafish photoreceptor outer segment development through a role in Rab8-dependent vesicle trafficking, Hum. Mol. Genet., 20, 4041, 10.1093/hmg/ddr332 Bech-Hansen, 1998, Loss-of-function mutations in a calcium-channel α1-subunit gene in Xp11.23 cause incomplete X-linked congenital stationary night blindness, Nat. Genet., 19, 264, 10.1038/947 Bergen, 2019, On the origin of proteins in human drusen: the meet, greet and stick hypothesis, Prog. Retin. Eye Res., 70, 55, 10.1016/j.preteyeres.2018.12.003 Bilotta, 2001, Rod contributions to the electroretinogram of the dark-adapted developing zebrafish, Dev. Dynam., 222, 564, 10.1002/dvdy.1188 Boldt, 2011, Disruption of intraflagellar protein transport in photoreceptor cilia causes Leber congenital amaurosis in humans and mice, J. Clin. Invest., 121, 2169, 10.1172/JCI45627 Booij, 2005, Identification of mutations in the AIPL1, CRB1, GUCY2D, RPE65, and RPGRIP1 genes in patients with juvenile retinitis pigmentosa, J. Med. Genet., 42, 1, 10.1136/jmg.2005.035121 Boubakri, 2016, Loss of ift122, a retrograde intraflagellar transport (IFT) complex component, leads to slow, progressive photoreceptor degeneration due to inefficient opsin transport, J. Biol. Chem., 291, 24465, 10.1074/jbc.M116.738658 Bowmaker, 1980, Visual pigments of rods and cones in a human retina, J. Physiol., 298, 501, 10.1113/jphysiol.1980.sp013097 Branchek, 1984, The development of photoreceptors in the zebrafish, brachydanio rerio. II. Function, J. Comp. Neurol. Branchek, 1984, The development of photoreceptors in the zebrafish, brachydanio rerio. I. Structure, J. Comp. Neurol., 224, 107, 10.1002/cne.902240109 Brockerhoff, 2011, Genetics of photoreceptor degeneration and regeneration in zebrafish, Cell. Mol. Life Sci., 68, 651, 10.1007/s00018-010-0563-8 Brockerhoff, 2003, Light stimulates a transducin-independent increase of cytoplasmic Ca2+ and suppression of current in cones from the zebrafish mutant nof, J. Neurosci., 23, 470, 10.1523/JNEUROSCI.23-02-00470.2003 Bujakowska, 2015, Mutations in IFT172 cause isolated retinal degeneration and Bardet-Biedl syndrome, Hum. Mol. Genet., 24, 230, 10.1093/hmg/ddu441 Campochiaro, 2018, The mechanism of cone cell death in retinitis pigmentosa Cantagrel, 2008, Mutations in the cilia gene ARL13B lead to the classical form of Joubert syndrome, Am. J. Hum. Genet., 83, 170, 10.1016/j.ajhg.2008.06.023 Cao, 2020, Effects of high-fat diet and Apoe deficiency on retinal structure and function in mice, Sci. Rep., 10, 1, 10.1038/s41598-020-75576-7 Cao, 2010, Hypoxia-induced retinopathy model in adult zebrafish, Nat. Protoc., 5, 1903, 10.1038/nprot.2010.149 Cardenas-Rodriguez, 2021, Genetic compensation for cilia defects in CEP290 mutants by upregulation of cilia-associated small GTPases, J. Cell Sci., 134, 10.1242/jcs.258568 Carr, 2021, Distinct roles for prominin-1 and photoreceptor cadherin in outer segment disc morphogenesis in CRISPR-altered X. laevis, J. Cell Sci., 134, jcs253906 Chakravarthy, 2010, Clinical risk factors for age-related macular degeneration: a systematic review and meta-analysis, BMC Ophthalmol., 10 Chang, 2009, A homologous genetic basis of the murine cpfl1 mutant and human achromatopsia linked to mutations in the PDE6C gene, Proc. Natl. Acad. Sci. U. S. A., 106, 19581, 10.1073/pnas.0907720106 Cheng, 2004, Photoreceptor-specific nuclear receptor NR2E3 functions as a transcriptional activator in rod photoreceptors, Hum. Mol. Genet., 13, 1563, 10.1093/hmg/ddh173 Cogné, 2020, Mutations in the kinesin-2 motor KIF3B cause an autosomal-dominant ciliopathy, Am. J. Hum. Genet., 106, 893, 10.1016/j.ajhg.2020.04.005 Collin, 2010, Mutations in C2ORF71 cause autosomal-recessive retinitis pigmentosa, Am. J. Hum. Genet., 86, 783, 10.1016/j.ajhg.2010.03.016 Coomer, 2020, Her9/Hes4 is required for retinal photoreceptor development, maintenance, and survival, Sci. Rep., 10, 1 Corless, 2012, Cone outer segments: a biophysical model of membrane dynamics, shape retention, and lamella formation, Biophys. J., 102, 2697, 10.1016/j.bpj.2012.04.052 Corral-Serrano, 2020, PCARE and WASF3 regulate ciliary F-actin assembly that is required for the initiation of photoreceptor outer segment disk formation, Proc. Natl. Acad. Sci. U. S. A., 117, 9922, 10.1073/pnas.1903125117 Corral-Serrano, 2018, C2orf71a/pcare1 is important for photoreceptor outer segment morphogenesis and visual function in zebrafish, Sci. Rep., 8, 1, 10.1038/s41598-018-27928-7 Cowan, 2020, Cell types of the human retina and its organoids at single-cell resolution, Cell, 182, 1623, 10.1016/j.cell.2020.08.013 Crouzier, 2021, Loss of Pde6a induces rod outer segment shrinkage and visual alterations in pde6a-Q70X mutant zebrafish, a relevant model of retinal dystrophy, Front. Cell Dev. Biol., 9, 10.3389/fcell.2021.675517 Curcio, 2005, Esterified and unesterified cholesterol in drusen and basal deposits of eyes with age-related maculopathy, Exp. Eye Res., 81, 731, 10.1016/j.exer.2005.04.012 Curcio, 1987, Distribution of cones in human and monkey retina: individual variability and radial asymmetry, Science, 236, 579, 10.1126/science.3576186 Daly, 2017, A brain-derived neurotrophic factor mimetic is sufficient to restore cone photoreceptor visual function in an inherited blindness model, Sci. Rep., 7, 1, 10.1038/s41598-017-11513-5 Daniele, 2016, Mutation of wrb, a component of the guided entry of tail-anchored protein pathway, disrupts photoreceptor synapse structure and function, Investig. Ophthal. Vis. Sc., 57, 2942, 10.1167/iovs.15-18996 Davey, 2006, The chicken talpid3 gene encodes a novel protein essential for Hedgehog signaling, Genes Dev., 20, 1365, 10.1101/gad.369106 Davidson, 2013, RP1L1 variants are associated with a spectrum of inherited retinal diseases including retinitis pigmentosa and occult macular dystrophy, Hum. Mutat., 34, 506, 10.1002/humu.22264 den Hollander, 2007, Mutations in LCA5, encoding the ciliary protein lebercilin, cause Leber congenital amaurosis, Nat. Genet., 39, 889, 10.1038/ng2066 den Hollander, 2006, Mutations in the CEP290 (NPHP6) gene are a frequent cause of Leber congenital amaurosis, Am. J. Hum. Genet., 79, 556, 10.1086/507318 DeWan, 2006, HTRA1 promoter polymorphism in wet age-related macular degeneration, Science, 314, 989, 10.1126/science.1133807 Dimopoulos, 2017, Choroideremia, Curr. Opin. Ophthalmol., 28, 410, 10.1097/ICU.0000000000000392 Doerre, 2002, Genetic analysis of photoreceptor cell development in the zebrafish retina, Mech. Dev., 110, 125, 10.1016/S0925-4773(01)00571-8 Dona, 2018, Usherin defects lead to early-onset retinal dysfunction in zebrafish, Exp. Eye Res., 173, 148, 10.1016/j.exer.2018.05.015 Doyon, 2008, Heritable targeted gene disruption in zebrafish using designed zinc-finger nucleases, Nat. Biotechnol., 26, 702, 10.1038/nbt1409 Dryja, 2001, Null RPGRIP1 alleles in patients with Leber congenital amaurosis, Am. J. Hum. Genet., 68, 1295, 10.1086/320113 Dryja, 1990, Mutations within the rhodopsin gene in patients with autosomal dominant retinitis pigmentosa, N. Engl. J. Med., 323, 1302, 10.1056/NEJM199011083231903 Dryja, 1990, A point mutation of the rhodopsin gene in one form of retinitis pigmentosa, Nature, 343, 364, 10.1038/343364a0 Dulla, 2021, Antisense oligonucleotide-based treatment of retinitis pigmentosa caused by USH2A exon 13 mutations, Mol. Ther., 29, 2441, 10.1016/j.ymthe.2021.04.024 Edvardson, 2010, Joubert syndrome 2 (JBTS2) in Ashkenazi Jews is associated with a TMEM216 mutation, Am. J. Hum. Genet., 86, 93, 10.1016/j.ajhg.2009.12.007 Eichers, 2002, Newfoundland rod-cone dystrophy, an early-onset retinal dystrophy, is caused by splice-junction mutations in RLBP1, Am. J. Hum. Genet., 70, 955, 10.1086/339688 El-Brolosy, 2019, Genetic compensation triggered by mutant mRNA degradation, Nature, 568, 193, 10.1038/s41586-019-1064-z Estrada-Cuzcano, 2012, BBS1 mutations in a wide spectrum of phenotypes ranging from nonsyndromic retinitis pigmentosa to bardet-biedl syndrome, Arch. Ophthalmol., 130, 1425, 10.1001/archophthalmol.2012.2434 Eudy, 1998, Mutation of a gene encoding a protein with extracellular matrix motifs in Usher syndrome type IIa, Science, 280, 1753, 10.1126/science.280.5370.1753 Fadool, 2003, Development of a rod photoreceptor mosaic revealed in transgenic zebrafish, Dev. Biol., 258, 277, 10.1016/S0012-1606(03)00125-8 Feng, 2017, The cytoplasmic tail of rhodopsin triggers rapid rod degeneration in kinesin-2 mutants, J. Biol. Chem., 292, 1735, 10.1074/jbc.M117.784017 Ferland, 2004, Abnormal cerebellar development and axonal decussation due to mutations in AHI1 in Joubert syndrome, Nat. Genet., 36, 1008, 10.1038/ng1419 Fischer, 2013, The ciliary marginal zone (CMZ) in development and regeneration of the vertebrate eye, Exp. Eye Res., 116, 199, 10.1016/j.exer.2013.08.018 Ganzen, 2021, Drug screening with zebrafish visual behavior identifies carvedilol as a potential treatment for an autosomal dominant form of retinitis pigmentosa, Sci. Rep., 11, 10.1038/s41598-021-89482-z Gao, 2022, Accumulation of lipid droplets in a novel Bietti crystalline dystrophy zebrafish model with impaired PPARα pathway, Investig. Opthalmol. Vis. Sci., 63, 32, 10.1167/iovs.63.5.32 Garcia-Gonzalo, 2011, A transition zone complex regulates mammalian ciliogenesis and ciliary membrane composition, Nat. Genet., 43, 776, 10.1038/ng.891 George, 2021, The retinal pigment epithelium: development, injury responses, and regenerative potential in mammalian and non-mammalian systems, Prog. Retin. Eye Res., 85, 10.1016/j.preteyeres.2021.100969 Goldberg, 2016, Molecular basis for photoreceptor outer segment architecture, Prog. Retin. Eye Res., 55, 52, 10.1016/j.preteyeres.2016.05.003 Goldman, 2014, Müller glial cell reprogramming and retina regeneration, Nat. Rev. Neurosci., 15, 431, 10.1038/nrn3723 Gopalakrishna, 2016, Aryl hydrocarbon receptor-interacting protein-like 1 is an obligate chaperone of phosphodiesterase 6 and is assisted by the γ-subunit of its client, J. Biol. Chem., 291, 16282, 10.1074/jbc.M116.737593 Gränse, 2001, Electrophysiological findings in two young patients with Bothnia dystrophy and a mutation in the RLBP1 gene, Ophthalmic Genet., 22, 97, 10.1076/opge.22.2.97.2231 Gross, 2005, Identification of zebrafish insertional mutants with defects in visual system development and function, Genetics, 170, 245, 10.1534/genetics.104.039727 Haider, 2000, Mutation of a nuclear receptor gene, NR2E3, causes enhanced S cone syndrome, a disorder of retinal cell fate, Nat. Genet., 24, 127, 10.1038/72777 Haider, 2009, Nr2e3-directed transcriptional regulation of genes involved in photoreceptor development and cell-type specific phototransduction, Exp. Eye Res., 89, 365, 10.1016/j.exer.2009.04.006 Hameed, 2003, Evidence of RPGRIP1 gene mutations associated with recessive cone-rod dystrophy, J. Med. Genet., 616, 10.1136/jmg.40.8.616 Han, 2018, Knockout of ush2a gene in zebrafish causes hearing impairment and late onset rod-cone dystrophy, Hum. Genet., 137, 779, 10.1007/s00439-018-1936-6 Han, 2012, Prominin-1 localizes to the open rims of outer segment lamellae in Xenopus laevis rod and cone photoreceptors, Investig. Ophthal. Vis. Sc., 53, 361, 10.1167/iovs.11-8635 Hejtmancik, 2008, Mutations in KCNJ13 cause autosomal-dominant snowflake vitreoretinal degeneration, Am. J. Hum. Genet., 82, 174, 10.1016/j.ajhg.2007.08.002 Hocking, 2018, Morphogenetic defects underlie Superior Coloboma, a newly identified closure disorder of the dorsal eye, PLoS Genet., 14, 10.1371/journal.pgen.1007246 Hodel, 2014, Myosin VIIA is a marker for the cone accessory outer segment in zebrafish, Anat. Rec., 297, 1777, 10.1002/ar.22976 Hofer, 2005, Organization of the human trichromatic cone mosaic, J. Neurosci., 25, 9669, 10.1523/JNEUROSCI.2414-05.2005 Holzhausen, 2009, Differential role for synaptojanin 1 in rod and cone photoreceptors, J. Comp. Neurol., 517, 633, 10.1002/cne.22176 Howe, 2013, The zebrafish reference genome sequence and its relationship to the human genome, Nature, 496, 498, 10.1038/nature12111 Huang, 2018, Zebrafish lacking circadian gene per2 exhibit visual function deficiency, Front. Behav. Neurosci., 12, 1, 10.3389/fnbeh.2018.00053 Huang, 1995, Autosomal recessive retinitis pigmentosa caused by mutations in the a subunit of rod cGMP phosphodiesterase, Nat. Genet., 11, 468, 10.1038/ng1295-468 Humbert, 2012, ARL13B, PDE6D, and CEP164 form a functional network for INPP5E ciliary targeting, Proc. Natl. Acad. Sci. U. S. A., 109, 19691, 10.1073/pnas.1210916109 Hwang, 2013, Efficient genome editing in zebrafish using a CRISPR-Cas system, Nat. Biotechnol., 31, 227, 10.1038/nbt.2501 Iribarne, 2017, Aipl1 is required for cone photoreceptor function and survival through the stability of Pde6c and Gc3 in zebrafish, Sci. Rep., 7, 1, 10.1038/srep45962 Jacobson, 1991, Retinal function and rhodopsin levels in autosomal dominant retinitis pigmentosa with rhodopsin mutations, Am. J. Ophthalmol., 112, 256, 10.1016/S0002-9394(14)76726-1 Jalkanen, 2006, X linked cone-rod dystrophy, CORDX3, is caused by a mutation in the CACNA1F gene, J. Med. Genet., 43, 699, 10.1136/jmg.2006.040741 Jia, 2014, Zebrafish cacna1fa is required for cone photoreceptor function and synaptic ribbon formation, Hum. Mol. Genet., 23, 2981, 10.1093/hmg/ddu009 Katagiri, 2014, Autosomal recessive cone-rod dystrophy associated with compound heterozygous mutations in the EYS gene, Doc. Ophthalmol., 128, 211, 10.1007/s10633-014-9435-0 Katsanis, 2001, Fundus albipunctatus and retinitis punctata albescens in a pedigree with an R150Q mutation in RLBP1, Clin. Genet., 59, 424, 10.1034/j.1399-0004.2001.590607.x Kohl, 2002, Mutations in the cone photoreceptor G-protein α-subunit gene GNAT2 in patients with achromatopsia, Am. J. Hum. Genet., 71, 422, 10.1086/341835 Kok, 2015, Reverse genetic screening reveals poor correlation between morpholino-induced and mutant phenotypes in zebrafish, Dev. Cell, 32, 97, 10.1016/j.devcel.2014.11.018 Krock, 2007, Noncell-autonomous photoreceptor degeneration in a zebrafish model of choroideremia, Proc. Natl. Acad. Sci. U. S. A., 104, 4600, 10.1073/pnas.0605818104 Krock, 2008, The intraflagellar transport protein IFT57 is required for cilia maintenance and regulates IFT-particle-kinesin-II dissociation in vertebrate photoreceptors, J. Cell Sci., 121, 1907, 10.1242/jcs.029397 Kroll, 2021, A simple and effective f0 knockout method for rapid screening of behaviour and other complex phenotypes, Elife, 10, 1, 10.7554/eLife.59683 Kumaran, 2017, Leber congenital amaurosis/early-onset severe retinal dystrophy: clinical features, molecular genetics and therapeutic interventions, Br. J. Ophthalmol., 101, 1147, 10.1136/bjophthalmol-2016-309975 Lee, 2014, Cluap1 is essential for ciliogenesis and photoreceptor maintenance in the vertebrate eye, Investig. Ophthal. Vis. Sc., 55, 4585, 10.1167/iovs.14-14888 Leitch, 2008, Hypomorphic mutations in syndromic encephalocele genes are associated with Bardet-Biedl syndrome, Nat. Genet., 40, 443, 10.1038/ng.97 Lenkowski, 2014, Müller glia: stem cells for generation and regeneration of retinal neurons in teleost fish, Prog. Retin. Eye Res., 40, 94, 10.1016/j.preteyeres.2013.12.007 Lessieur, 2017, The ciliopathy gene ahi1 is required for zebrafish cone photoreceptor outer segment morphogenesis and survival, Investig. Ophthal. Vis. Sc., 58, 448, 10.1167/iovs.16-20326 Lessieur, 2019, Ciliary genes arl13b, ahi1 and cc2d2a differentially modify expression of visual acuity phenotypes but do not enhance retinal degeneration due to mutation of cep290 in zebrafish, PLoS One, 14, 1, 10.1371/journal.pone.0213960 Li, 2004, Bietti crystalline corneoretinal dystrophy is caused by mutations in the novel gene CYP4V2, Am. J. Hum. Genet., 74, 817, 10.1086/383228 Li, 2020, Fluoride impairs ovary development by affecting oogenesis and inducing oxidative stress and apoptosis in female zebrafish (Danio rerio), Chemosphere, 256, 10.1016/j.chemosphere.2020.127105 Li, 2014, Comprehensive analysis of gene expression in human retina and supporting tissues, Hum. Mol. Genet., 23, 4001, 10.1093/hmg/ddu114 Lin, 2018, HTRA1, an age-related macular degeneration protease, processes extracellular matrix proteins EFEMP1 and TSP1, Aging Cell, 17, 10.1111/acel.12710 Lin, 2016, The zebrafish pinball wizard gene encodes WRB, a tail-anchored-protein receptor essential for inner-ear hair cells and retinal photoreceptors, J. Physiol., 594, 895, 10.1113/JP271437 Lindstrand, 2016, Copy-number variation contributes to the mutational load of Bardet-Biedl Syndrome, Am. J. Hum. Genet., 99, 318, 10.1016/j.ajhg.2015.04.023 Littink, 2018, Autosomal recessive NRL mutations in patients with enhanced S-cone syndrome, Genes, 9, 1, 10.3390/genes9020068 Liu, 2015, Knockout of RP2 decreases GRK1 and rod transducin subunits and leads to photoreceptor degeneration in zebrafish, Hum. Mol. Genet., 24, 4648, 10.1093/hmg/ddv197 Liu, 2022, Rod genesis driven by mafba in an nrl knockout zebrafish model with altered photoreceptor composition and progressive retinal degeneration, PLoS Genet., 18, 10.1371/journal.pgen.1009841 Liu, 2020, TMEM216 deletion causes mislocalization of cone opsin and rhodopsin and photoreceptor degeneration in zebrafish, Investig. Ophthal. Vis. Sc., 61, 1, 10.1167/iovs.61.3.1 Liu, 2020, Eyes shut homolog (EYS) interacts with matriglycan of O-mannosyl glycans whose deficiency results in EYS mislocalization and degeneration of photoreceptors, Sci. Rep., 10, 1 Lobo, 2017, The exocyst is required for photoreceptor ciliogenesis and retinal development, J. Biol. Chem., 292, 14814, 10.1074/jbc.M117.795674 Lu, 2017, Ablation of EYS in zebrafish causes mislocalisation of outer segment proteins, F-actin disruption and cone-rod dystrophy, Sci. Rep., 7, 1 Lu, 2019, Deletion of the transmembrane protein Prom1b in zebrafish disrupts outer-segment morphogenesis and causes photoreceptor degeneration, J. Biol. Chem., 294, 13953, 10.1074/jbc.RA119.008618 Luo, 2021, Disrupted intraflagellar transport due to IFT74 variants causes Joubert syndrome, Genet. Med., 23, 1041, 10.1038/s41436-021-01106-z Madelaine, 2017, Endogenous retinal neural stem cell reprogramming for neuronal regeneration, Neural Regener. Res., 12, 1765, 10.4103/1673-5374.219028 Marszalek, 1999, Situs inversus and embryonic ciliary morphogenesis defects in mouse mutants lacking the KIF3A subunit of kinesin-II, Devop. Biol. Martins, 2022, Müller Glia maintain their regenerative potential despite degeneration in the aged zebrafish retina, Aging Cell, 10.1111/acel.13597 Masek, 2022, Loss of the Bardet-Biedl protein Bbs1 alters photoreceptor outer segment protein and lipid composition, Nat. Commun., 13, 10.1038/s41467-022-28982-6 Maw, 1997 May-Simera, 2017, Cilia - the sensory antennae in the eye, Prog. Retin. Eye Res., 60, 144, 10.1016/j.preteyeres.2017.05.001 Mears, 2001, Nrl is required for rod photoreceptor development, Nat. Genet., 29, 447, 10.1038/ng774 Merry, 1992, Isolation of a candidate gene for choroideremia, Genetics, 89, 2135 Michaelides, 2010, The PROM1 mutation p.R373C causes an autosomal dominant bull's eye maculopathy associated with rod, rod-cone, and macular dystrophy, Investig. Ophthal. Vis. Sc., 51, 4771, 10.1167/iovs.09-4561 Miles, 2021, Usher syndrome type 1-associated gene, pcdh15b, is required for photoreceptor structural integrity in zebrafish, Dis. Model. Mech., 14, 10.1242/dmm.048965 Morris, 2011, Microarray analysis of XOPS-mCFP zebrafish retina identifies genes associated with rod photoreceptor degeneration and regeneration, Investig. Ophthal. Vis. Sc., 52, 2255, 10.1167/iovs.10-6022 Morris, 2005, Cone survival despite rod degeneration in XOPS-mCFP transgenic zebrafish, Investig. Ophthalmol. Vis. Sci., 46, 4762, 10.1167/iovs.05-0797 Morshedian, 2017 Mustafi, 2009, Structure of cone photoreceptors, Prog. Retin. Eye Res., 28, 289, 10.1016/j.preteyeres.2009.05.003 Mykytyn, 2003, Evaluation of complex inheritance involving the most common Bardet-Biedl syndrome locus (BBS1), Am. J. Hum. Genet., 72, 429, 10.1086/346172 Mykytyn, 2002, Identification of the gene (BBS1) most commonly involved in Bardet-Biedl syndrome, a complex human obesity syndrome, Nat. Genet., 31, 435, 10.1038/ng935 Nadolski, 2020, Abnormal cone and rod photoreceptor morphogenesis in gdf6a mutant zebrafish, Investig. Ophthal. Vis. Sc., 61 Naharros, 2018, The ciliopathy protein TALPID3/KIAA0586 acts upstream of Rab8 activation in zebrafish photoreceptor outer segment formation and maintenance, Sci. Rep., 8, 1 Nakao, 2012, The role of mislocalized phototransduction in photoreceptor cell death of retinitis pigmentosa, PLoS One, 7, 10.1371/journal.pone.0032472 Narayan, 2016, A review of the mechanisms of cone degeneration in retinitis pigmentosa, Acta Ophthalmol., 94, 748, 10.1111/aos.13141 Neuhauss, 2003, Behavioral genetic approaches to visual system development and function in zebrafish, J. Neurobiol., 54, 148, 10.1002/neu.10165 Newman, 2016, Homozygosity for a recessive loss-of-function mutation of the NRL gene is associated with a variant of enhanced S-cone syndrome, Investig. Ophthal. Vis. Sc., 57, 5361, 10.1167/iovs.16-19505 Nishiguchi, 2004, Recessive NRL mutations in patients with clumped pigmentary retinal degeneration and relative preservation of blue cone function, Proc. Natl. Acad. Sci. USA, 101, 17819, 10.1073/pnas.0408183101 Nishimura, 2010, Discovery and functional analysis of a retinitis pigmentosa gene, C2ORF71, Am. J. Hum. Genet., 86, 686, 10.1016/j.ajhg.2010.03.005 Nishimura, 2001, Positional cloning of a novel gene on chromosome 16q causing Bardet-Biedl syndrome (BBS2), Hum. Mol. Genet., 10.1093/hmg/10.8.865 Nishimura, 2001, Positional cloning of a novel gene on chromosome 16q causing Bardet-Biedl syndrome (BBS2), Hum. Mol. Genet., 10, 865, 10.1093/hmg/10.8.865 Nishiwaki, 2008, Mutation of cGMP phosphodiesterase 6α′-subunit gene causes progressive degeneration of cone photoreceptors in zebrafish, Mech. Dev., 125, 932, 10.1016/j.mod.2008.09.001 Nishiwaki, 2013, The BH3-only SNARE BNip1 mediates photoreceptor apoptosis in response to vesicular fusion defects, Dev. Cell, 25, 374, 10.1016/j.devcel.2013.04.015 Noel, 2018, Connectivity of cone photoreceptor telodendria in the zebrafish retina, J. Comp. Neurol., 526, 609, 10.1002/cne.24354 Noel, 2020, RP1L1 and inherited photoreceptor disease: a review, Surv. Ophthalmol., 65, 725, 10.1016/j.survophthal.2020.04.005 Noel, 2020, Progressive photoreceptor dysfunction and age-related macular degeneration-like features in rp1l1 mutant zebrafish, Cells, 9, 2214, 10.3390/cells9102214 Noor, 2008, CC2D2A, encoding a coiled-coil and C2 domain protein, causes autosomal-recessive mental retardation with retinitis pigmentosa, Am. J. Hum. Genet., 82, 1011, 10.1016/j.ajhg.2008.01.021 Oel, 2020, Nrl is dispensable for specification of rod photoreceptors in adult zebrafish despite its deeply conserved requirement earlier in ontogeny, iScience, 23, 10.1016/j.isci.2020.101805 Oura, 2018, High-temperature requirement A 1 causes photoreceptor cell death in zebrafish disease models, Am. J. Pathol., 188, 2729, 10.1016/j.ajpath.2018.08.012 Patton, 2001, The art and design of genetic screens: Zebrafish, Nat. Rev. Genet., 2, 956, 10.1038/35103567 Pooranachandran, 2016, Unexpected roles for ciliary kinesins and intraflagellar transport proteins, Genetics, 203, 771, 10.1534/genetics.115.180943 Qu, 2019, Knocking out lca5 in zebrafish causes cone-rod dystrophy due to impaired outer segment protein trafficking, Biochim. Biophys. Acta (BBA) - Mol. Basis Dis., 1865, 2694, 10.1016/j.bbadis.2019.07.009 Raghupathy, 2016, Abnormal photoreceptor outer segment development and early retinal degeneration in kif3a mutant zebrafish, Cell Biochem. Funct., 34, 429, 10.1002/cbf.3205 Raghupathy, 2017, Rpgrip1 is required for rod outer segment development and ciliary protein trafficking in zebrafish, Sci. Rep., 7, 1, 10.1038/s41598-017-12838-x RetNet, https://sph.uth.edu/RetNet/[WWW Document], (n.d). Ripps, 2002, Cell death in retinitis pigmentosa: gap junctions and the “bystander” effect, Exp. Eye Res., 74, 327, 10.1006/exer.2002.1155 Rivolta, 2002, Paternal uniparental heterodisomy with partial isodisomy of chromosome 1 in a patient with retinitis pigmentosa without hearing loss and a missense mutation in the Usher syndrome type II gene USH2A, Ophthal. Mol. Genet., 120, 1566 Rivolta, 2001, Dominant leber congenital amaurosis, cone-rod degeneration, and retinitis pigmentosa caused by mutant versions of the transcription factor CRX, Hum. Mutat., 18, 488, 10.1002/humu.1226 Robinson, 1995, Temporal and spatial patterns of opsin gene expression in zebrafish (Danio rerio), Vis. Neurosci., 12, 895, 10.1017/S0952523800009457 Roddy, 2020, Diet mimicking “fast food” causes structural changes to the retina relevant to age-related macular degeneration, Curr. Eye Res., 45, 726, 10.1080/02713683.2019.1694156 Rohrer, 2021, Conditional loss of the exocyst component exoc5 in retinal pigment epithelium (RPE) results in RPE dysfunction, photoreceptor cell degeneration, and decreased visual function, Int. J. Mol. Sci., 22, 10.3390/ijms22105083 Rosenfeld, 1992, A Null mutation in the rhodopsin gene causes rod photoreceptor dysfunction and autosomal recessive retinitis pigmentosa, Nat. Genet., 1, 209, 10.1038/ng0692-209 Rossi, 2015, Genetic compensation induced by deleterious mutations but not gene knockdowns, Nature, 524, 230, 10.1038/nature14580 Santhanam, 2020, A zebrafish model of retinitis pigmentosa shows continuous degeneration and regeneration of rod photoreceptors, Cells, 9, 10.3390/cells9102242 Sayer, 2006, The centrosomal protein nephrocystin-6 is mutated in Joubert syndrome and activates transcription factor ATF4, Nat. Genet., 38, 674, 10.1038/ng1786 Schellens, 2021, Zebrafish as a model to evaluate a CRISPR/Cas9-based exon excision approach as a future treatment option for EYS-associated retinitis pigmentosa, Int. J. Mol. Sci., 22, 9154, 10.3390/ijms22179154 Schietroma, 2017, Usher syndrome type 1-associated cadherins shape the photoreceptor outer segment, JCB (J. Cell Biol.), 216, 1849, 10.1083/jcb.201612030 Schlegel, 2019, A new zebrafish model for CACNA2D4-dysfunction, Investig. Ophthal. Vis. Sc., 60, 5124, 10.1167/iovs.19-26759 Schlegel, 2021, Disturbed retinoid metabolism upon loss of rlbp1a impairs cone function and leads to subretinal lipid deposits and photoreceptor degeneration in the zebrafish retina, Elife, 10, 1, 10.7554/eLife.71473 Schwahn, 1998, Positional cloning of the gene for X-linked retinitis pigmentosa 2, Nat. Genet., 19, 327, 10.1038/1214 Seabra, 1993, Retinal degeneration in choroideremia: deficiency of Rab geranylgeranyl transferase, Science, 259, 377, 10.1126/science.8380507 Sergouniotis, 2011, Recessive mutations in KCNJ13, encoding an inwardly rectifying potassium channel subunit, cause Leber congenital amaurosis, Am. J. Hum. Genet., 89, 183, 10.1016/j.ajhg.2011.06.002 Serra, 2019, Mutations in c2orf71 causing an early onset form of cone-rod dystrophy: a molecular diagnosis after 20 years of clinical follow-up, Mol. Vis., 25, 814 Shevach, 2015, Association between missense mutations in the BBS2 gene and nonsyndromic retinitis pigmentosa, JAMA Ophthal., 133, 312, 10.1001/jamaophthalmol.2014.5251 Soens, 2016, Hypomorphic mutations identified in the candidate Leber congenital amaurosis gene CLUAP1, Genet. Med., 18, 1044, 10.1038/gim.2015.205 Sohocki, 2000, Prevalence of AIPL1 mutations in inherited retinal degenerative disease, Mol. Genet. Metabol., 70, 142, 10.1006/mgme.2000.3001 Sohocki, 2000, Mutations in a new photoreceptor-pineal gene on 17p cause Leber congenital amaurosis, Nat. Genet., 24, 79, 10.1038/71732 Sohocki, 2000, Mutations in a new photoreceptor-pineal gene on 17p cause Leber congenital amaurosis, Nat. Genet., 24, 79, 10.1038/71732 Song, 2016, Arl13b interacts with vangl2 to regulate cilia and photoreceptor outer segment length in zebrafish, Investig. Ophthal. Vis. Sc., 57, 4517, 10.1167/iovs.16-19898 Song, 2020, Cone photoreceptor degeneration and neuroinflammation in the zebrafish Bardet-Biedl syndrome 2 (bbs2) mutant does not lead to retinal regeneration, Front. Cell Dev. Biol., 8, 1, 10.3389/fcell.2020.578528 Spaide, 2018, Subretinal drusenoid deposits AKA pseudodrusen, Surv. Ophthalmol., 63, 782, 10.1016/j.survophthal.2018.05.005 Stearns, 2007, A mutation in the cone-specific pde6 gene causes rapid cone photoreceptor degeneration in zebrafish, J. Neurosci., 27, 13866, 10.1523/JNEUROSCI.3136-07.2007 Strom, 1998, An L-type calcium-channel gene mutated in incomplete X-linked congenital stationary night blindness, Nat. Genet., 19, 260, 10.1038/940 Sukumaran, 2009, Early defects in photoreceptor outer segment morphogenesis in zebrafish ift57, ift88 and ift172 intraflagellar transport mutants, Vis. Res., 49, 479, 10.1016/j.visres.2008.12.009 Sung, 2010, The cell biology of vision, JCB (J. Cell Biol.), 190, 953, 10.1083/jcb.201006020 Sung, 1994, A rhodopsin gene mutation responsible for autosomal dominant retinitis pigmentosa results in a protein that is defective in localization to the photoreceptor outer segment, J. Neurosci., 14, 5818, 10.1523/JNEUROSCI.14-10-05818.1994 Thiadens, 2009, Homozygosity mapping reveals PDE6C mutations in patients with early-onset cone photoreceptor disorders, Am. J. Hum. Genet., 85, 240, 10.1016/j.ajhg.2009.06.016 Thornton, 2005, Smoking and age-related macular degeneration: a review of association, Eye, 19, 935, 10.1038/sj.eye.6701978 Toms, 2019, Phagosomal and mitochondrial alterations in RPE may contribute to KCNJ13 retinopathy, Sci. Rep., 9, 1, 10.1038/s41598-019-40507-8 Trojan, 2008, Centrins in retinal photoreceptor cells: regulators in the connecting cilium, Prog. Retin. Eye Res., 27, 237, 10.1016/j.preteyeres.2008.01.003 Tsujikawa, 2004, Intraflagellar transport genes are essential for differentiation and survival of vertebrate sensory neurons, Neuron, 42, 703, 10.1016/S0896-6273(04)00268-5 Tuson, 2004, Mutation of CERKL, a novel human ceramide kinase gene, causes autosomal recessive retinitis pigmentosa (RP26), Am. J. Hum. Genet., 74, 128, 10.1086/381055 Valente, 2010, Mutations in TMEM216 perturb ciliogenesis and cause Joubert, Meckel and related syndromes, Nat. Genet., 42, 619, 10.1038/ng.594 Valente, 2006, Mutations in CEP290, which encodes a centrosomal protein, cause pleiotropic forms of Joubert syndrome, Nat. Genet., 38, 623, 10.1038/ng1805 van Epps, 2004, The zebrafish nrc mutant reveals a role for the polyphosphoinositide phosphatase synaptojanin 1 in cone photoreceptor ribbon anchoring, J. Neurosci., 24, 8641, 10.1523/JNEUROSCI.2892-04.2004 van houcke, 2019, Extensive growth is followed by neurodegenerative pathology in the continuously expanding zebrafish retina, Biogerontology, 20, 109, 10.1007/s10522-018-9780-6 van Rooijen, 2010, Von Hippel-Lindau tumor suppressor mutants faithfully model pathological hypoxia-driven angiogenesis and vascular retinopathies in zebrafish, Dis. Model. Mech., 3, 343, 10.1242/dmm.004036 Verdura, 2015, Heterozygous HTRA1 mutations are associated with autosomal dominant cerebral small vessel disease, Brain, 138, 2347, 10.1093/brain/awv155 Viringipurampeer, 2014, Rip3 knockdown rescues photoreceptor cell death in blind pde6c zebrafish, Cell Death Differ., 21, 665, 10.1038/cdd.2013.191 Vithana, 2001, A human homolog of yeast pre-mRNA splicing gene, PRP31, underlies autosomal dominant retinitis pigmentosa on chromosome 19q13.4 (RP11), Mol. Cell, 8, 375, 10.1016/S1097-2765(01)00305-7 Wan, 2016, Retina regeneration in zebrafish, Curr. Opin. Genet. Dev., 40, 41, 10.1016/j.gde.2016.05.009 Wan, 2016, The ciliary marginal zone of the zebrafish retina: clonal and time-lapse analysis of a continuously growing tissue, Development, 143, 1099 Wasfy, 2014, Myosin 7aa-/- mutant zebrafish show mild photoreceptor degeneration and reduced electroretinographic responses, Exp. Eye Res., 122, 65, 10.1016/j.exer.2014.03.007 Weil, 1997, The autosomal recessive isolated deafness, DFNB2, and the Usher 1B syndrome are allelic defects of the myosin-VIIA gene, Nat. Genet., 16, 191, 10.1038/ng0697-191 Whiteheart, 1993, SNAP family of NSF attachment proteins includes a brain-specific isoform, Nature Lett., 362, 353, 10.1038/362353a0 Wu, 2015, The exocyst at a glance, J. Cell Sci., 128, 2957 Wycisk, 2006, Mutation in the auxiliary calcium-channel subunit CACNA2D4 causes autosomal recessive cone dystrophy, Am. J. Hum. Genet., 79, 973, 10.1086/508944 Xie, 2019, Knockout of Nr2e3 prevents rod photoreceptor differentiation and leads to selective L-/M-cone photoreceptor degeneration in zebrafish, Biochim. Biophys. Acta (BBA) - Mol. Basis Dis., 1865, 1273, 10.1016/j.bbadis.2019.01.022 Xu, 2016, Mutations in POMGNT1 cause non-syndromic retinitis pigmentosa, Hum. Mol. Genet., 25, 1479, 10.1093/hmg/ddw022 Yamamoto, 2012, Molecular machinery for insertion of tail-anchored membrane proteins into the endoplasmic reticulum membrane in mammalian cells, Mol. Cell, 48, 387, 10.1016/j.molcel.2012.08.028 Yang, 2006, A variant of the HTRA1 gene increases susceptibility to age-related macular degeneration, Science, 314, 992, 10.1126/science.1133811 Yang, 2008, Mutant prominin 1 found in patients with macular degeneration disrupts photoreceptor disk morphogenesis in mice, J. Clin. Invest., 118, 2908 Yang, 2008, Mutant prominin 1 found in patients with macular degeneration disrupts photoreceptor disk morphogenesis in mice, J. Clin. Invest., 118, 2908 Yin, 2011, Mutant Prpf31 causes pre-mRNA splicing defects and rod photoreceptor cell degeneration in a zebrafish model for retinitis pigmentosa, Mol. Neurodegener., 6, 56, 10.1186/1750-1326-6-56 Yin, 2009, The Talpid3 gene (KIAA0586) encodes a centrosomal protein that is essential for primary cilia formation, Development, 136, 655, 10.1242/dev.028464 Yoshimatsu, 2020, Fovea-like photoreceptor specializations underlie single UV cone driven prey-capture behavior in zebrafish, Neuron, 107, 320, 10.1016/j.neuron.2020.04.021 Yu, 2016, Eyes shut homolog is required for maintaining the ciliary pocket and survival of photoreceptors in zebrafish, Biology Open, 5, 1662, 10.1242/bio.021584 Yu, 2017, CERKL gene knockout disturbs photoreceptor outer segment phagocytosis and causes rod-cone dystrophy in zebrafish, Hum. Mol. Genet., 26, 2335, 10.1093/hmg/ddx137 Yurco, 2005, Responses of Muller glia to retinal injury in adult zebrafish, Vis. Res., 45, 991, 10.1016/j.visres.2004.10.022 Zelinka, 2018, Targeted disruption of the endogenous zebrafish rhodopsin locus as models of rapid rod photoreceptor degeneration, Mol. Vis., 24, 587 Zhang, 2021, Large-scale phenotypic drug screen identifies neuroprotectants in zebrafish and mouse models of retinitis pigmentosa, Elife, 10, 10.7554/eLife.57245 Zhang, 2016, A naturally-derived compound schisandrin B enhanced light sensation in the pde6c zebrafish model of retinal degeneration, PLoS One, 11, 1 Zhang, 2018, Pgc-1α repression and high-fat diet induce age-related macular degeneration-like phenotypes in mice, Dis. Model. Mech., 11, 10.1242/dmm.032698 Zhang, 2007, Severe retinitis pigmentosa mapped to 4p15 and associated with a novel mutation in the PROM1 gene, Hum. Genet., 122, 293, 10.1007/s00439-007-0395-2 Zhao, 2012, Kinesin-2 family in vertebrate ciliogenesis, Proc. Natl. Acad. Sci. U. S. A., 109, 2388, 10.1073/pnas.1116035109 Zhao, 2021, Environmentally relevant concentration of cypermethrin or/and sulfamethoxazole induce neurotoxicity of grass carp: involvement of blood-brain barrier, oxidative stress and apoptosis, Sci. Total Environ., 762, 10.1016/j.scitotenv.2020.143054 Zhu, 2021, Loss of Ift74 leads to Slow photoreceptor degeneration and ciliogenesis defects in zebrafish, Int. J. Mol. Sci., 22, 9329, 10.3390/ijms22179329 Zu, 2013, TALEN-mediated precise genome modification by homologous recombination in zebrafish, Nat. Methods, 10, 329, 10.1038/nmeth.2374 Zuo, 2009, The exocyst protein Sec10 is necessary for primary ciliogenesis and cystogenesis in vitro, Mol. Biol. Cell, 20, 2522, 10.1091/mbc.e08-07-0772