XB-ART-53081
Curr Pathobiol Rep
2017 Jan 01;51:67-78. doi: 10.1007/s40139-017-0127-9.
Show Gene links
Show Anatomy links
Retinal Degeneration and Regeneration-Lessons From Fishes and Amphibians.
Ail D
,
Perron M
.
???displayArticle.abstract???
PURPOSE OF REVIEW: Retinal degenerative diseases have immense socio-economic impact. Studying animal models that recapitulate human eye pathologies aids in understanding the pathogenesis of diseases and allows for the discovery of novel therapeutic strategies. Some non-mammalian species are known to have remarkable regenerative abilities and may provide the basis to develop strategies to stimulate self-repair in patients suffering from these retinal diseases. RECENT FINDINGS: Non-mammalian organisms, such as zebrafish and Xenopus, have become attractive model systems to study retinal diseases. Additionally, many fish and amphibian models of retinal cell ablation and cell lineage analysis have been developed to study regeneration. These investigations highlighted several cellular sources for retinal repair in different fish and amphibian species. Moreover, major differences in repair mechanisms have been reported in these animal models. SUMMARY: This review aims to emphasize first on the importance of zebrafish and Xenopus models in studying the pathogenesis of retinal diseases and, second, on the different modes of regeneration processes in these model organisms.
???displayArticle.pubmedLink??? 28255526
???displayArticle.pmcLink??? PMC5309292
???displayArticle.link??? Curr Pathobiol Rep
???attribute.lit??? ???displayArticles.show???
|
|
Fig. 1. a Structure of the retina. Schematic representation of a cross section of the zebrafish or Xenopus eye showing the ciliary marginal zone (CMZ), retinal pigment epithelium (RPE), neural retina, choroid, Bruch’s membrane, and the retinal vascular membrane (RVM). b Cell types of the retina. The retina is composed of different cell types: the nuclei of the two types of photoreceptors, rods (R) and cones (C), form the outer nuclear layer (ONL), whereas the Müller cells (M), horizontal cells (H), bipolar cells (B), and amacrine cells (A) are present in the inner nuclear layer (INL), and the ganglion cells (G) in the ganglion cell layer (GCL). The axons of these neurons and glial cells form synaptic connections in the outer and inner plexiform layers (OPL and IPL). The astrocytes (As) are located near the blood vessels whereas the microglia (Mi) are mostly located in the plexiform layers but can be distributed through the different layers. c–e Modes of regeneration and repair. CMZ-mediated (c): In the constantly growing retinas of zebrafish and Xenopus, the spatial cellular gradient in the CMZ recapitulates embryonic retinogenesis with zone I, the most peripheral part of the CMZ, where stem cells reside, zone II encompassing retinal progenitor cells, and zone III consisting of late retinal progenitors including post-mitotic retinoblasts. The stem cells divide asymmetrically to self-renew and generate one progenitor cell, and this mode of asymmetric division is retained even in the case of retinal injury. RPE-mediated (d): In Xenopus following partial retinectomy, wherein the RPE and RVM are left intact (a), a subset of RPE cells (green oval cells) detach from the Bruch’s membrane (in red) and migrate to the RVM (b). When they adhere to the RVM and form a distinct layer of cells (blue cells), they start proliferating (c) and regenerate the whole neural retina (d), while RPE cells that remained attached to the Bruch’s membrane renew the RPE layer (d). Müller-cell mediated (e): In zebrafish upon retinal injury, a subset of Müller cells (orange) undergo asymmetric division (black) to renew themselves and generate multipotent progenitor cells that can actively divide and regenerate all major retinal cell types (color figure online) |
References [+] :
Agathocleous,
From progenitors to differentiated cells in the vertebrate retina.
2009, Pubmed
Agathocleous, From progenitors to differentiated cells in the vertebrate retina. 2009, Pubmed
Agbaga, Mutant ELOVL4 that causes autosomal dominant stargardt-3 macular dystrophy is misrouted to rod outer segment disks. 2014, Pubmed , Xenbase
Alvarez, Predominant cone photoreceptor dysfunction in a hyperglycaemic model of non-proliferative diabetic retinopathy. 2010, Pubmed
Amato, Comparison of the expression patterns of five neural RNA binding proteins in the Xenopus retina. 2005, Pubmed , Xenbase
Araki, Regeneration of the amphibian retina: role of tissue interaction and related signaling molecules on RPE transdifferentiation. 2007, Pubmed , Xenbase
Arango-Gonzalez, Identification of a common non-apoptotic cell death mechanism in hereditary retinal degeneration. 2014, Pubmed
Bainbridge, Long-term effect of gene therapy on Leber's congenital amaurosis. 2015, Pubmed
Bennett, Current Progress in Deciphering Importance of VLC-PUFA in the Retina. 2016, Pubmed
Bernardos, Late-stage neuronal progenitors in the retina are radial Müller glia that function as retinal stem cells. 2007, Pubmed
Bernstein, Lutein, zeaxanthin, and meso-zeaxanthin: The basic and clinical science underlying carotenoid-based nutritional interventions against ocular disease. 2016, Pubmed
Bibliowicz, Toward a better understanding of human eye disease insights from the zebrafish, Danio rerio. 2011, Pubmed
Bogéa, Light Induces Ultrastructural Changes in Rod Outer and Inner Segments, Including Autophagy, in a Transgenic Xenopus laevis P23H Rhodopsin Model of Retinitis Pigmentosa. 2015, Pubmed , Xenbase
Borday, Antagonistic cross-regulation between Wnt and Hedgehog signalling pathways controls post-embryonic retinal proliferation. 2012, Pubmed , Xenbase
Bringmann, Müller cells in the healthy and diseased retina. 2006, Pubmed
Buchholz, Derivation of functional retinal pigmented epithelium from induced pluripotent stem cells. 2009, Pubmed
Cameron, Cellular proliferation and neurogenesis in the injured retina of adult zebrafish. 2000, Pubmed
Cao, Hypoxia-induced retinal angiogenesis in zebrafish as a model to study retinopathy. 2008, Pubmed
Cao, Hypoxia-induced retinopathy model in adult zebrafish. 2010, Pubmed
Carr, Protective effects of human iPS-derived retinal pigment epithelium cell transplantation in the retinal dystrophic rat. 2009, Pubmed
Casarosa, Genetic analysis of metamorphic and premetamorphic Xenopus ciliary marginal zone. 2005, Pubmed , Xenbase
Centanin, Exclusive multipotency and preferential asymmetric divisions in post-embryonic neural stem cells of the fish retina. 2014, Pubmed
Centanin, Fate restriction and multipotency in retinal stem cells. 2011, Pubmed
Cerveny, Continued growth and circuit building in the anamniote visual system. 2012, Pubmed
Chhetri, Zebrafish--on the move towards ophthalmological research. 2014, Pubmed
Chiba, The retinal pigment epithelium: an important player of retinal disorders and regeneration. 2014, Pubmed , Xenbase
Chohan, Müller stem cell dependent retinal regeneration. 2017, Pubmed
Choi, Cone degeneration following rod ablation in a reversible model of retinal degeneration. 2011, Pubmed , Xenbase
Curado, Nitroreductase-mediated cell/tissue ablation in zebrafish: a spatially and temporally controlled ablation method with applications in developmental and regeneration studies. 2008, Pubmed
D'Orazi, Mismatch of Synaptic Patterns between Neurons Produced in Regeneration and during Development of the Vertebrate Retina. 2016, Pubmed
Dejneka, In utero gene therapy rescues vision in a murine model of congenital blindness. 2004, Pubmed
DiCicco, Retinal regeneration following OCT-guided laser injury in zebrafish. 2014, Pubmed
Dixon, VEGF Trap-Eye for the treatment of neovascular age-related macular degeneration. 2009, Pubmed
El Yakoubi, Hes4 controls proliferative properties of neural stem cells during retinal ontogenesis. 2012, Pubmed , Xenbase
Fausett, A role for alpha1 tubulin-expressing Müller glia in regeneration of the injured zebrafish retina. 2006, Pubmed
Fausett, The proneural basic helix-loop-helix gene ascl1a is required for retina regeneration. 2008, Pubmed
Ferreiro-Galve, Patterns of cell proliferation and rod photoreceptor differentiation in shark retinas. 2010, Pubmed
Filoni, Retina and lens regeneration in anuran amphibians. 2009, Pubmed , Xenbase
Fimbel, Regeneration of inner retinal neurons after intravitreal injection of ouabain in zebrafish. 2007, Pubmed
Fischer, Identification of a proliferating marginal zone of retinal progenitors in postnatal chickens. 2000, Pubmed
Fischer, The ciliary marginal zone (CMZ) in development and regeneration of the vertebrate eye. 2013, Pubmed
Fraser, Regeneration of cone photoreceptors when cell ablation is primarily restricted to a particular cone subtype. 2013, Pubmed
Gleeson, Induction of hyperglycaemia in zebrafish (Danio rerio) leads to morphological changes in the retina. 2007, Pubmed
Gonzalez-Cordero, Photoreceptor precursors derived from three-dimensional embryonic stem cell cultures integrate and mature within adult degenerate retina. 2013, Pubmed
Gorsuch, Regulation of Müller glial dependent neuronal regeneration in the damaged adult zebrafish retina. 2014, Pubmed
Grassmann, The genetics of age-related macular degeneration (AMD)--Novel targets for designing treatment options? 2015, Pubmed
Hamm, Controlled rod cell ablation in transgenic Xenopus laevis. 2009, Pubmed , Xenbase
Hamon, Müller glial cell-dependent regeneration of the neural retina: An overview across vertebrate model systems. 2016, Pubmed
Harris, Molecular recapitulation: the growth of the vertebrate retina. 1998, Pubmed
Heon, Mutations in C8ORF37 cause Bardet Biedl syndrome (BBS21). 2016, Pubmed
Hirami, Generation of retinal cells from mouse and human induced pluripotent stem cells. 2009, Pubmed
Hitchcock, Local regeneration in the retina of the goldfish. 1992, Pubmed
Hollyfield, Differential growth of the neural retina in Xenopus laevis larvae. 1971, Pubmed , Xenbase
Hollyfield, Differential addition of cells to the retina in Rana pipiens tadpoles. 1968, Pubmed
Hurley, Glucose, lactate, and shuttling of metabolites in vertebrate retinas. 2015, Pubmed
Jayakody, Cellular strategies for retinal repair by photoreceptor replacement. 2015, Pubmed
Jin, Opsin activation as a cause of congenital night blindness. 2003, Pubmed , Xenbase
Johns, Formation of photoreceptors in larval and adult goldfish. 1982, Pubmed
Johns, Growth of the adult goldfish eye. III. Source of the new retinal cells. 1977, Pubmed
Kassen, Time course analysis of gene expression during light-induced photoreceptor cell death and regeneration in albino zebrafish. 2007, Pubmed
Kiyama, Distinct neurogenic potential in the retinal margin and the pars plana of mammalian eye. 2012, Pubmed
Kubota, A comparative study of neurogenesis in the retinal ciliary marginal zone of homeothermic vertebrates. 2002, Pubmed
Kuriyama, Complete reconstruction of the retinal laminar structure from a cultured retinal pigment epithelium is triggered by altered tissue interaction and promoted by overlaid extracellular matrices. 2009, Pubmed , Xenbase
Kurz-Isler, Morphological study on the regeneration of the retina in the rainbow trout after ouabain-induced damage: evidence for dedifferentiation of photoreceptors. 1982, Pubmed
Kuwahara, Generation of a ciliary margin-like stem cell niche from self-organizing human retinal tissue. 2015, Pubmed
Lahne, Actin-Cytoskeleton- and Rock-Mediated INM Are Required for Photoreceptor Regeneration in the Adult Zebrafish Retina. 2015, Pubmed
Lahne, Interkinetic Nuclear Migration in the Regenerating Retina. 2016, Pubmed
Lambert, Risk factors and biomarkers of age-related macular degeneration. 2016, Pubmed
Lee, Fourier domain optical coherence tomography as a noninvasive means for in vivo detection of retinal degeneration in Xenopus laevis tadpoles. 2010, Pubmed , Xenbase
Lee, Dysmorphic photoreceptors in a P23H mutant rhodopsin model of retinitis pigmentosa are metabolically active and capable of regenerating to reverse retinal degeneration. 2012, Pubmed , Xenbase
Lee, Xenopus laevis tadpoles can regenerate neural retina lost after physical excision but cannot regenerate photoreceptors lost through targeted ablation. 2013, Pubmed , Xenbase
Lenkowski, Müller glia: Stem cells for generation and regeneration of retinal neurons in teleost fish. 2014, Pubmed
Link, Zebrafish Models of Retinal Disease. 2015, Pubmed
Luo, The Argus(®) II Retinal Prosthesis System. 2016, Pubmed
Lust, De novo neurogenesis by targeted expression of atoh7 to Müller glia cells. 2016, Pubmed
Maier, Regeneration of the goldfish retina after exposure to different doses of ouabain. 1979, Pubmed
Martinez-De Luna, The Retinal Homeobox (Rx) gene is necessary for retinal regeneration. 2011, Pubmed , Xenbase
Maurer, Methylnitrosourea (MNU)-induced retinal degeneration and regeneration in the zebrafish: histological and functional characteristics. 2014, Pubmed
Mitchell, A systematic review of the efficacy and safety outcomes of anti-VEGF agents used for treating neovascular age-related macular degeneration: comparison of ranibizumab and bevacizumab. 2011, Pubmed
Miyake, Retinal stem/progenitor cells in the ciliary marginal zone complete retinal regeneration: a study of retinal regeneration in a novel animal model. 2014, Pubmed , Xenbase
Montgomery, A novel model of retinal ablation demonstrates that the extent of rod cell death regulates the origin of the regenerated zebrafish rod photoreceptors. 2010, Pubmed
Moshiri, Retinal stem cells and regeneration. 2004, Pubmed
Nagashima, A self-renewing division of zebrafish Müller glial cells generates neuronal progenitors that require N-cadherin to regenerate retinal neurons. 2013, Pubmed
Negishi, Paradoxical induction of dopaminergic cells following intravitreal injection of high doses of 6-hydroxydopamine in juvenile carp retina. 1987, Pubmed
Nelson, Tumor necrosis factor-alpha is produced by dying retinal neurons and is required for Muller glia proliferation during zebrafish retinal regeneration. 2013, Pubmed
Nelson, Müller glia as a source of neuronal progenitor cells to regenerate the damaged zebrafish retina. 2012, Pubmed
Ogai, Cell Fate of Müller Cells During Photoreceptor Regeneration in an N-Methyl-N-nitrosourea-Induced Retinal Degeneration Model of Zebrafish. 2016, Pubmed
Ohnuma, Co-ordinating retinal histogenesis: early cell cycle exit enhances early cell fate determination in the Xenopus retina. 2002, Pubmed , Xenbase
Otteson, Putative stem cells and the lineage of rod photoreceptors in the mature retina of the goldfish. 2001, Pubmed
Pearson, Restoration of vision after transplantation of photoreceptors. 2012, Pubmed
Pearson, Donor and host photoreceptors engage in material transfer following transplantation of post-mitotic photoreceptor precursors. 2016, Pubmed
Perron, The genetic sequence of retinal development in the ciliary margin of the Xenopus eye. 1998, Pubmed , Xenbase
Powell, Zebrafish Müller glia-derived progenitors are multipotent, exhibit proliferative biases and regenerate excess neurons. 2016, Pubmed
Rajaram, Technical brief: Constant intense light exposure to lesion and initiate regeneration in normally pigmented zebrafish. 2014, Pubmed
Ramachandran, Insm1a-mediated gene repression is essential for the formation and differentiation of Müller glia-derived progenitors in the injured retina. 2012, Pubmed
Ramachandran, Ascl1a regulates Müller glia dedifferentiation and retinal regeneration through a Lin-28-dependent, let-7 microRNA signalling pathway. 2010, Pubmed
Raymond, Regeneration: New Neurons Wire Up. 2016, Pubmed
Raymond, Molecular characterization of retinal stem cells and their niches in adult zebrafish. 2006, Pubmed
Raymond, Regeneration of goldfish retina: rod precursors are a likely source of regenerated cells. 1988, Pubmed
Reh, Cell-specific regulation of neuronal production in the larval frog retina. 1987, Pubmed
Reh, Photoreceptor Transplantation in Late Stage Retinal Degeneration. 2016, Pubmed
Rezzola, Zebrafish (Danio rerio) embryo as a platform for the identification of novel angiogenesis inhibitors of retinal vascular diseases. 2016, Pubmed
STONE, Regeneration of neural retina and lens from retina pigment cell grafts in adult newts. 1957, Pubmed
Salero, Adult human RPE can be activated into a multipotent stem cell that produces mesenchymal derivatives. 2012, Pubmed
Santos-Ferreira, Retinal transplantation of photoreceptors results in donor-host cytoplasmic exchange. 2016, Pubmed
Schwartz, Human embryonic stem cell-derived retinal pigment epithelium in patients with age-related macular degeneration and Stargardt's macular dystrophy: follow-up of two open-label phase 1/2 studies. 2015, Pubmed
Schwartz, Embryonic stem cell trials for macular degeneration: a preliminary report. 2012, Pubmed
Seddon, The epidemiology of age-related macular degeneration. 2004, Pubmed
Senut, An element in the alpha1-tubulin promoter is necessary for retinal expression during optic nerve regeneration but not after eye injury in the adult zebrafish. 2004, Pubmed
Sherpa, Retinal regeneration is facilitated by the presence of surviving neurons. 2014, Pubmed
Shirai, Transplantation of human embryonic stem cell-derived retinal tissue in two primate models of retinal degeneration. 2016, Pubmed
Sifuentes, Rapid, Dynamic Activation of Müller Glial Stem Cell Responses in Zebrafish. 2016, Pubmed
Siqueira, Intravitreal injection of autologous bone marrow-derived mononuclear cells for hereditary retinal dystrophy: a phase I trial. 2011, Pubmed
Song, Treatment of macular degeneration using embryonic stem cell-derived retinal pigment epithelium: preliminary results in Asian patients. 2015, Pubmed
Song, Arl13b Interacts With Vangl2 to Regulate Cilia and Photoreceptor Outer Segment Length in Zebrafish. 2016, Pubmed
Stearns, A mutation in the cone-specific pde6 gene causes rapid cone photoreceptor degeneration in zebrafish. 2007, Pubmed
Stenkamp, Evidence for two distinct mechanisms of neurogenesis and cellular pattern formation in regenerated goldfish retinas. 2001, Pubmed
Stenkamp, The rod photoreceptor lineage of teleost fish. 2011, Pubmed
Stoetzel, A mutation in VPS15 (PIK3R4) causes a ciliopathy and affects IFT20 release from the cis-Golgi. 2016, Pubmed
Straznicky, The growth of the retina in Xenopus laevis: an autoradiographic study. 1971, Pubmed , Xenbase
Sánchez-Farías, Identification of Radial Glia Progenitors in the Developing and Adult Retina of Sharks. 2016, Pubmed
Tam, Generation of transgenic X. laevis models of retinal degeneration. 2013, Pubmed , Xenbase
Tam, Characterization of rhodopsin P23H-induced retinal degeneration in a Xenopus laevis model of retinitis pigmentosa. 2006, Pubmed , Xenbase
Tam, Photoactivation-induced instability of rhodopsin mutants T4K and T17M in rod outer segments underlies retinal degeneration in X. laevis transgenic models of retinitis pigmentosa. 2014, Pubmed , Xenbase
Tam, Dark rearing rescues P23H rhodopsin-induced retinal degeneration in a transgenic Xenopus laevis model of retinitis pigmentosa: a chromophore-dependent mechanism characterized by production of N-terminally truncated mutant rhodopsin. 2007, Pubmed , Xenbase
Tappeiner, Inhibition of the TGFβ Pathway Enhances Retinal Regeneration in Adult Zebrafish. 2016, Pubmed
Tappeiner, Characteristics of rod regeneration in a novel zebrafish retinal degeneration model using N-methyl-N-nitrosourea (MNU). 2013, Pubmed
Thomas, Characterization of multiple light damage paradigms reveals regional differences in photoreceptor loss. 2012, Pubmed
Thomas, Reactive gliosis in the adult zebrafish retina. 2016, Pubmed
Thummel, Inhibition of Müller glial cell division blocks regeneration of the light-damaged zebrafish retina. 2008, Pubmed
Thummel, Characterization of Müller glia and neuronal progenitors during adult zebrafish retinal regeneration. 2008, Pubmed
Todd, Comparative analysis of glucagonergic cells, glia, and the circumferential marginal zone in the reptilian retina. 2016, Pubmed
Tsubura, Animal models for retinitis pigmentosa induced by MNU; disease progression, mechanisms and therapeutic trials. 2010, Pubmed
Turner, A common progenitor for neurons and glia persists in rat retina late in development. , Pubmed
Ueda, Transgenic Xenopus laevis with the ef1-α promoter as an experimental tool for amphibian retinal regeneration study. 2012, Pubmed , Xenbase
Ueki, Transgenic expression of the proneural transcription factor Ascl1 in Müller glia stimulates retinal regeneration in young mice. 2015, Pubmed
Vergara, Retinal regeneration in the Xenopus laevis tadpole: a new model system. 2009, Pubmed , Xenbase
Vihtelic, Light-induced rod and cone cell death and regeneration in the adult albino zebrafish (Danio rerio) retina. 2000, Pubmed
Vihtelic, Retinal regional differences in photoreceptor cell death and regeneration in light-lesioned albino zebrafish. 2006, Pubmed
Viringipurampeer, Rip3 knockdown rescues photoreceptor cell death in blind pde6c zebrafish. 2014, Pubmed
Wan, Retina regeneration in zebrafish. 2016, Pubmed
Wan, Retinal injury, growth factors, and cytokines converge on β-catenin and pStat3 signaling to stimulate retina regeneration. 2014, Pubmed
Wan, The ciliary marginal zone of the zebrafish retina: clonal and time-lapse analysis of a continuously growing tissue. 2016, Pubmed
Weber, Characterization of light lesion paradigms and optical coherence tomography as tools to study adult retina regeneration in zebrafish. 2013, Pubmed
Wehman, Genetic dissection of the zebrafish retinal stem-cell compartment. 2005, Pubmed
Wetts, Cell lineage analysis reveals multipotent precursors in the ciliary margin of the frog retina. 1989, Pubmed , Xenbase
Wheway, An siRNA-based functional genomics screen for the identification of regulators of ciliogenesis and ciliopathy genes. 2015, Pubmed
Wilson, Tracking the fate of her4 expressing cells in the regenerating retina using her4:Kaede zebrafish. 2016, Pubmed
Yoshii, Neural retinal regeneration in the anuran amphibian Xenopus laevis post-metamorphosis: transdifferentiation of retinal pigmented epithelium regenerates the neural retina. 2007, Pubmed , Xenbase
Yoshimatsu, Transmission from the dominant input shapes the stereotypic ratio of photoreceptor inputs onto horizontal cells. 2014, Pubmed
van Rooijen, von Hippel-Lindau tumor suppressor mutants faithfully model pathological hypoxia-driven angiogenesis and vascular retinopathies in zebrafish. 2010, Pubmed