1932

Abstract

In humans, various genetic defects or age-related diseases, such as diabetic retinopathies, glaucoma, and macular degeneration, cause the death of retinal neurons and profound vision loss. One approach to treating these diseases is to utilize stem and progenitor cells to replace neurons in situ, with the expectation that new neurons will create new synaptic circuits or integrate into existing ones. Reprogramming non-neuronal cells in vivo into stem or progenitor cells is one strategy for replacing lost neurons. Zebrafish have become a valuable model for investigating cellular reprogramming and retinal regeneration. This review summarizes our current knowledge regarding spontaneous reprogramming of Müller glia in zebrafish and compares this knowledge to research efforts directed toward reprogramming Müller glia in mammals. Intensive research using these animal models has revealed shared molecular mechanisms that make Müller glia attractive targets for cellular reprogramming and highlighted the potential for curing degenerative retinal diseases from intrinsic cellular sources.

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2020-09-15
2024-04-19
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Literature Cited

  1. Aldiri I, Moore KB, Hutcheson DA, Zhang J, Vetter ML 2013. Polycomb repressive complex PRC2 regulates Xenopus retina development downstream of Wnt/beta-catenin signaling. Development 140:142867–78
    [Google Scholar]
  2. Ariga J, Walker SL, Mumm JS 2010. Multicolor time-lapse imaging of transgenic zebrafish: visualizing retinal stem cells activated by targeted neuronal cell ablation. J. Vis. Exp. 43:2093
    [Google Scholar]
  3. Bailey TJ, Fossum SL, Fimbel SM, Montgomery JE, Hyde DR 2010. The inhibitor of phagocytosis, O-phospho-L-serine, suppresses Muller glia proliferation and cone cell regeneration in the light-damaged zebrafish retina. Exp. Eye Res. 91:5601–12
    [Google Scholar]
  4. Battista AG, Ricatti MJ, Pafundo DE, Gautier MA, Faillace MP 2009. Extracellular ADP regulates lesion-induced in vivo cell proliferation and death in the zebrafish retina. J. Neurochem. 111:2600–13
    [Google Scholar]
  5. Bernardos RL, Barthel LK, Meyers JR, Raymond PA 2007. Late-stage neuronal progenitors in the retina are radial Muller glia that function as retinal stem cells. J. Neurosci. 27:267028–40
    [Google Scholar]
  6. Blackshaw S, Harpavat S, Trimarchi J, Cai L, Huang H et al. 2004. Genomic analysis of mouse retinal development. PLOS Biol 2:9E247
    [Google Scholar]
  7. Bracken AP, Dietrich N, Pasini D, Hansen KH, Helin K 2006. Genome-wide mapping of Polycomb target genes unravels their roles in cell fate transitions. Genes Dev 20:91123–36
    [Google Scholar]
  8. Braisted JE, Raymond PA. 1993. Continued search for the cellular signals that regulate regeneration of dopaminergic neurons in goldfish retina. Dev. Brain Res. 76:2221–32
    [Google Scholar]
  9. Bringmann A, Iandiev I, Pannicke T, Wurm A, Hollborn M et al. 2009. Cellular signaling and factors involved in Muller cell gliosis: neuroprotective and detrimental effects. Prog. Retin. Eye Res. 28:6423–51
    [Google Scholar]
  10. Bringmann A, Pannicke T, Grosche J, Francke M, Wiedemann P et al. 2006. Muller cells in the healthy and diseased retina. Prog. Retin. Eye Res. 25:4397–424
    [Google Scholar]
  11. Conedera FM, Quintela Pousa AM, Mercader N, Tschopp M, Enzmann V 2019. Retinal microglia signaling affects Muller cell behavior in the zebrafish following laser injury induction. Glia 67:61150–66
    [Google Scholar]
  12. Conner C, Ackerman KM, Lahne M, Hobgood JS, Hyde DR 2014. Repressing Notch signaling and expressing TNFalpha are sufficient to mimic retinal regeneration by inducing Muller glial proliferation to generate committed progenitor cells. J. Neurosci. 34:4314403–19
    [Google Scholar]
  13. Corso-Diaz X, Jaeger C, Chaitankar V, Swaroop A 2018. Epigenetic control of gene regulation during development and disease: a view from the retina. Prog. Retin. Eye Res. 65:1–27
    [Google Scholar]
  14. Craig SE, Calinescu AA, Hitchcock PF 2008. Identification of the molecular signatures integral to regenerating photoreceptors in the retina of the zebra fish. J. Ocul. Biol. Dis. Inform. 1:2–473–84
    [Google Scholar]
  15. Del Debbio CB, Balasubramanian S, Parameswaran S, Chaudhuri A, Qiu F, Ahmad I 2010. Notch and Wnt signaling mediated rod photoreceptor regeneration by Muller cells in adult mammalian retina. PLOS ONE 5:8e12425
    [Google Scholar]
  16. Du J, Johnson LM, Jacobsen SE, Patel DJ 2015. DNA methylation pathways and their crosstalk with histone methylation. Nat. Rev. Mol. Cell Biol. 16:9519–32
    [Google Scholar]
  17. Duncan EA, Anest V, Cogswell P, Baldwin AS 2006. The kinases MSK1 and MSK2 are required for epidermal growth factor-induced, but not tumor necrosis factor-induced, histone H3 Ser10 phosphorylation. J. Biol. Chem. 281:1812521–25
    [Google Scholar]
  18. Dyer MA, Cepko CL. 2000. Control of Muller glial cell proliferation and activation following retinal injury. Nat. Neurosci. 3:9873–80
    [Google Scholar]
  19. Elsaeidi F, Macpherson P, Mills EA, Jui J, Flannery JG, Goldman D 2018. Notch suppression collaborates with Ascl1 and Lin28 to unleash a regenerative response in fish retina, but not in mice. J. Neurosci. 38:92246–61
    [Google Scholar]
  20. Fausett BV, Goldman D. 2006. A role for alpha1 tubulin-expressing Muller glia in regeneration of the injured zebrafish retina. J. Neurosci. 26:236303–13
    [Google Scholar]
  21. Fausett BV, Gumerson JD, Goldman D 2008. The proneural basic helix-loop-helix gene ascl1a is required for retina regeneration. J. Neurosci. 28:51109–17
    [Google Scholar]
  22. Fimbel SM, Montgomery JE, Burket CT, Hyde DR 2007. Regeneration of inner retinal neurons after intravitreal injection of ouabain in zebrafish. J. Neurosci. 27:71712–24
    [Google Scholar]
  23. Fischer AJ, Reh TA. 2001. Muller glia are a potential source of neural regeneration in the postnatal chicken retina. Nat. Neurosci. 4:3247–52
    [Google Scholar]
  24. Fischer AJ, Reh TA. 2002. Exogenous growth factors stimulate the regeneration of ganglion cells in the chicken retina. Dev. Biol. 251:2367–79
    [Google Scholar]
  25. Fischer AJ, Scott MA, Tuten W 2009. Mitogen-activated protein kinase-signaling stimulates Müller glia to proliferate in acutely damaged chicken retina. Glia 57:2166–81
    [Google Scholar]
  26. Fischer AJ, Zelinka C, Scott MA 2010. Heterogeneity of glia in the retina and optic nerve of birds and mammals. PLOS ONE 5:6e10774
    [Google Scholar]
  27. Fraser B, DuVal MG, Wang H, Allison WT 2013. Regeneration of cone photoreceptors when cell ablation is primarily restricted to a particular cone subtype. PLOS ONE 8:1e55410
    [Google Scholar]
  28. Furukawa T, Mukherjee S, Bao ZZ, Morrow EM, Cepko CL 2000. rax, Hes1, and notch1 promote the formation of Muller glia by postnatal retinal progenitor cells. Neuron 26:2383–94
    [Google Scholar]
  29. Galan A, Dergham P, Escoll P, de-la-Hera A, D'Onofrio PM et al. 2014. Neuronal injury external to the retina rapidly activates retinal glia, followed by elevation of markers for cell cycle re-entry and death in retinal ganglion cells. PLOS ONE 9:7e101349
    [Google Scholar]
  30. Gallina D, Palazzo I, Steffenson L, Todd L, Fischer AJ 2016. Wnt/beta-catenin-signaling and the formation of Muller glia-derived progenitors in the chick retina. Dev. Neurobiol. 76:9983–1002
    [Google Scholar]
  31. Gehani SS, Agrawal-Singh S, Dietrich N, Christophersen NS, Helin K, Hansen K 2010. Polycomb group protein displacement and gene activation through MSK-dependent H3K27me3S28 phosphorylation. Mol. Cell 39:6886–900
    [Google Scholar]
  32. Ghai K, Zelinka C, Fischer AJ 2010. Notch signaling influences neuroprotective and proliferative properties of mature Muller glia. J. Neurosci. 30:83101–12
    [Google Scholar]
  33. Gökbuget D, Blelloch R. 2019. Epigenetic control of transcriptional regulation in pluripotency and early differentiation. Development 146:19
    [Google Scholar]
  34. Goldman D. 2014. Muller glial cell reprogramming and retina regeneration. Nat. Rev. Neurosci. 15:7431–42
    [Google Scholar]
  35. Gorsuch RA, Hyde DR. 2014. Regulation of Muller glial dependent neuronal regeneration in the damaged adult zebrafish retina. Exp. Eye Res. 123:131–40
    [Google Scholar]
  36. Gorsuch RA, Lahne M, Yarka CE, Petravick ME, Li J, Hyde DR 2017. Sox2 regulates Muller glia reprogramming and proliferation in the regenerating zebrafish retina via Lin28 and Ascl1a. Exp. Eye Res. 161:174–92
    [Google Scholar]
  37. Gotz M, Sirko S, Beckers J, Irmler M 2015. Reactive astrocytes as neural stem or progenitor cells: in vivo lineage, in vitro potential, and genome-wide expression analysis. Glia 63:81452–68
    [Google Scholar]
  38. Graca AB, Hippert C, Pearson RA 2018. Muller glia reactivity and development of gliosis in response to pathological conditions. Adv. Exp. Med. Biol. 1074:303–8
    [Google Scholar]
  39. Hagerman GF, Noel NC, Cao SY, DuVal MG, Oel AP, Allison WT 2016. Rapid recovery of visual function associated with blue cone ablation in zebrafish. PLOS ONE 11:11e0166932
    [Google Scholar]
  40. Hamon A, Garcia-Garcia D, Ail D, Bitard J, Chesneau A et al. 2019. Linking YAP to Muller glia quiescence exit in the degenerative retina. Cell Rep 27:61712–1725.e6
    [Google Scholar]
  41. Hamon A, Roger JE, Yang XJ, Perron M 2016. Muller glial cell-dependent regeneration of the neural retina: an overview across vertebrate model systems. Dev. Dyn. 245:7727–38
    [Google Scholar]
  42. Hayes S, Nelson BR, Buckingham B, Reh TA 2007. Notch signaling regulates regeneration in the avian retina. Dev. Biol. 312:1300–11
    [Google Scholar]
  43. Hitchcock PF, Raymond PA. 2004. The teleost retina as a model for developmental and regeneration biology. Zebrafish 1:3257–71
    [Google Scholar]
  44. Ho DM, Artavanis-Tsakonas S, Louvi A 2019. The Notch pathway in CNS homeostasis and neurodegeneration. Wiley Interdiscip. Rev. Dev. Biol. 9:e358
    [Google Scholar]
  45. Hoang T, Wang J, Boyd P, Wang F, Santiago C et al. 2019. Cross-species transcriptomic and epigenomic analysis reveals key regulators of injury response and neuronal regeneration in vertebrate retinas. bioRxiv 717876. https://doi.org/10.1101/717876
    [Crossref]
  46. Huynh J, Etemadi N, Hollande F, Ernst M, Buchert M 2017. The JAK/STAT3 axis: a comprehensive drug target for solid malignancies. Semin. Cancer Biol. 45:13–22
    [Google Scholar]
  47. Insua MF, Simon MV, Garelli A, de Los Santos B, Rotstein NP, Politi LE 2008. Trophic factors and neuronal interactions regulate the cell cycle and Pax6 expression in Muller stem cells. J. Neurosci. Res. 86:71459–71
    [Google Scholar]
  48. Iribarne M, Hyde DR, Masai I 2019. TNFα induces Müller glia to transition from non-proliferative gliosis to a regenerative response in mutant zebrafish presenting chronic photoreceptor degeneration. Front. Cell Dev. Biol. 7:296
    [Google Scholar]
  49. Iribarne M, Nishiwaki Y, Nakamura S, Araragi M, Oguri E, Masai I 2017. Aipl1 is required for cone photoreceptor function and survival through the stability of Pde6c and Gc3 in zebrafish. Sci. Rep. 7:45962
    [Google Scholar]
  50. Jadhav AP, Roesch K, Cepko CL 2009. Development and neurogenic potential of Muller glial cells in the vertebrate retina. Prog. Retin. Eye Res. 28:4249–62
    [Google Scholar]
  51. Jeong JJ, Gu X, Nie J, Sundaravel S, Liu H et al. 2019. Cytokine-regulated phosphorylation and activation of TET2 by JAK2 in hematopoiesis. Cancer Discov 9:6778–95
    [Google Scholar]
  52. Jiang K, Wright KL, Zhu P, Szego MJ, Bramall AN et al. 2014. STAT3 promotes survival of mutant photoreceptors in inherited photoreceptor degeneration models. PNAS 111:52E5716–23
    [Google Scholar]
  53. Johns PR. 1977. Growth of the adult goldfish eye. III. Source of the new retinal cells. J. Comp. Neurol. 176:3343–57
    [Google Scholar]
  54. Johns PR, Fernald RD. 1981. Genesis of rods in teleost fish retina. Nature 293:5828141–42
    [Google Scholar]
  55. Joly S, Pernet V, Samardzija M, Grimm C 2011. Pax6-positive Müller glia cells express cell cycle markers but do not proliferate after photoreceptor injury in the mouse retina. Glia 59:71033–46
    [Google Scholar]
  56. Jorstad NL, Wilken MS, Grimes WN, Wohl SG, VandenBosch LS et al. 2017. Stimulation of functional neuronal regeneration from Muller glia in adult mice. Nature 548:7665103–7
    [Google Scholar]
  57. Karl MO, Hayes S, Nelson BR, Tan K, Buckingham B, Reh TA 2008. Stimulation of neural regeneration in the mouse retina. PNAS 105:4919508–13
    [Google Scholar]
  58. Karl MO, Reh TA. 2010. Regenerative medicine for retinal diseases: activating endogenous repair mechanisms. Trends Mol. Med. 16:4193–202
    [Google Scholar]
  59. Kase S, Yoshida K, Harada T, Harada C, Namekata K et al. 2006. Phosphorylation of extracellular signal-regulated kinase and p27(KIP1) after retinal detachment. Graefe's Arch. Clin. Exp. Ophthalmol. 244:3352–58
    [Google Scholar]
  60. Kassen SC, Ramanan V, Montgomery JE, Burket CT, Liu CG et al. 2007. Time course analysis of gene expression during light-induced photoreceptor cell death and regeneration in albino zebrafish. Dev. Neurobiol. 67:81009–31
    [Google Scholar]
  61. Kassen SC, Thummel R, Campochiaro LA, Harding MJ, Bennett NA, Hyde DR 2009. CNTF induces photoreceptor neuroprotection and Muller glial cell proliferation through two different signaling pathways in the adult zebrafish retina. Exp. Eye Res. 88:61051–64
    [Google Scholar]
  62. Kaur S, Gupta S, Chaudhary M, Khursheed MA, Mitra S et al. 2018. let-7 microRNA-mediated regulation of Shh signaling and the gene regulatory network is essential for retina regeneration. Cell Rep 23:51409–23
    [Google Scholar]
  63. Kirsch M, Trautmann N, Ernst M, Hofmann H 2010. Involvement of gp130-associated cytokine signaling in Müller cell activation following optic nerve lesion. Glia 58:7768–79
    [Google Scholar]
  64. Kizil C, Kyritsis N, Brand M 2015. Effects of inflammation on stem cells: together they strive. EMBO Rep 16:4416–26
    [Google Scholar]
  65. Kyritsis N, Kizil C, Zocher S, Kroehne V, Kaslin J et al. 2012. Acute inflammation initiates the regenerative response in the adult zebrafish brain. Science 338:61121353–56
    [Google Scholar]
  66. Lahne M, Hyde DR. 2017. Live-cell imaging: new avenues to investigate retinal regeneration. Neural Regen. Res. 12:1210–19
    [Google Scholar]
  67. Lahne M, Li J, Marton RM, Hyde DR 2015. Actin-cytoskeleton- and Rock-mediated INM are required for photoreceptor regeneration in the adult zebrafish retina. J. Neurosci. 35:4715612–34
    [Google Scholar]
  68. Lenkowski JR, Raymond PA. 2014. Muller glia: stem cells for generation and regeneration of retinal neurons in teleost fish. Prog. Retin. Eye Res. 40:94–123
    [Google Scholar]
  69. Lessieur EM, Song P, Nivar GC, Piccillo EM, Fogerty J et al. 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 14:4e0213960
    [Google Scholar]
  70. Lewis GP, Chapin EA, Luna G, Linberg KA, Fisher SK 2010. The fate of Muller's glia following experimental retinal detachment: nuclear migration, cell division, and subretinal glial scar formation. Mol. Vis. 16:1361–72
    [Google Scholar]
  71. Li L, Dowling JE. 2000. Effects of dopamine depletion on visual sensitivity of zebrafish. J. Neurosci. 20:51893–903
    [Google Scholar]
  72. Lluis F, Cosma MP. 2010. Cell-fusion-mediated somatic-cell reprogramming: a mechanism for tissue regeneration. J. Cell. Physiol. 223:16–13
    [Google Scholar]
  73. Lluis F, Pedone E, Pepe S, Cosma MP 2008. Periodic activation of Wnt/beta-catenin signaling enhances somatic cell reprogramming mediated by cell fusion. Cell Stem Cell 3:5493–507
    [Google Scholar]
  74. Maier W, Wolburg H. 1979. Regeneration of the goldfish retina after exposure to different doses of ouabain. Cell Tissue Res 202:199–118
    [Google Scholar]
  75. Medrano MP, Bejarano CA, Battista AG, Venera GD, Bernabeu RO, Faillace MP 2017. Injury-induced purinergic signalling molecules upregulate pluripotency gene expression and mitotic activity of progenitor cells in the zebrafish retina. Purinergic Signal 13:4443–65
    [Google Scholar]
  76. Meyers JR, Hu L, Moses A, Kaboli K, Papandrea A, Raymond PA 2012. β-Catenin/Wnt signaling controls progenitor fate in the developing and regenerating zebrafish retina. Neural Dev 7:30
    [Google Scholar]
  77. Mitra S, Sharma P, Kaur S, Khursheed MA, Gupta S et al. 2018. Histone deacetylase-mediated Muller glia reprogramming through Her4.1-Lin28a axis is essential for retina regeneration in zebrafish. iScience 7:68–84
    [Google Scholar]
  78. Mitra S, Sharma P, Kaur S, Khursheed MA, Gupta S et al. 2019. Dual regulation of lin28a by Myc is necessary during zebrafish retina regeneration. J. Cell Biol. 218:2489–507
    [Google Scholar]
  79. Mizeracka K, DeMaso CR, Cepko CL 2013. Notch1 is required in newly postmitotic cells to inhibit the rod photoreceptor fate. Development 140:153188–97
    [Google Scholar]
  80. Montgomery JE, Parsons MJ, Hyde DR 2010. A novel model of retinal ablation demonstrates that the extent of rod cell death regulates the origin of the regenerated zebrafish rod photoreceptors. J. Comp. Neurol. 518:6800–14
    [Google Scholar]
  81. Morris AC, Scholz TL, Brockerhoff SE, Fadool JM 2008. Genetic dissection reveals two separate pathways for rod and cone regeneration in the teleost retina. Dev. Neurobiol. 68:5605–19
    [Google Scholar]
  82. Nagashima M, Barthel LK, Raymond PA 2013. A self-renewing division of zebrafish Muller glial cells generates neuronal progenitors that require N-cadherin to regenerate retinal neurons. Development 140:224510–21
    [Google Scholar]
  83. Nagashima M, D'Cruz TS, Danku AE, Hesse D, Sifuentes C et al. 2020. Midkine-a is required for cell cycle progression of Müller glia during neuronal regeneration in the vertebrate retina. J. Neurosci. 40:6123247
    [Google Scholar]
  84. Nakazawa T, Takeda M, Lewis GP, Cho KS, Jiao J et al. 2007. Attenuated glial reactions and photoreceptor degeneration after retinal detachment in mice deficient in glial fibrillary acidic protein and vimentin. Investig. Ophthalmol. Vis. Sci. 48:62760–68
    [Google Scholar]
  85. Nelson CM, Ackerman KM, O'Hayer P, Bailey TJ, Gorsuch RA, Hyde DR 2013. Tumor necrosis factor-alpha is produced by dying retinal neurons and is required for Muller glia proliferation during zebrafish retinal regeneration. J. Neurosci. 33:156524–39
    [Google Scholar]
  86. Nelson CM, Gorsuch RA, Bailey TJ, Ackerman KM, Kassen SC, Hyde DR 2012. Stat3 defines three populations of Muller glia and is required for initiating maximal Muller glia proliferation in the regenerating zebrafish retina. J. Comp. Neurol. 520:184294–311
    [Google Scholar]
  87. O'Meara MM, Simon JA. 2012. Inner workings and regulatory inputs that control Polycomb repressive complex 2. Chromosoma 121:3221–34
    [Google Scholar]
  88. Ooto S, Akagi T, Kageyama R, Akita J, Mandai M et al. 2004. Potential for neural regeneration after neurotoxic injury in the adult mammalian retina. PNAS 101:3713654–59
    [Google Scholar]
  89. Otteson DC, D'Costa AR, Hitchcock PF 2001. Putative stem cells and the lineage of rod photoreceptors in the mature retina of the goldfish. Dev. Biol. 232:162–76
    [Google Scholar]
  90. Pollak J, Wilken MS, Ueki Y, Cox KE, Sullivan JM et al. 2013. ASCL1 reprograms mouse Muller glia into neurogenic retinal progenitors. Development 140:122619–31
    [Google Scholar]
  91. Powell C, Cornblath E, Elsaeidi F, Wan J, Goldman D 2016. Zebrafish Muller glia-derived progenitors are multipotent, exhibit proliferative biases and regenerate excess neurons. Sci. Rep. 6:24851
    [Google Scholar]
  92. Powell C, Elsaeidi F, Goldman D 2012. Injury-dependent Muller glia and ganglion cell reprogramming during tissue regeneration requires Apobec2a and Apobec2b. J. Neurosci. 32:31096–109
    [Google Scholar]
  93. Powell C, Grant AR, Cornblath E, Goldman D 2013. Analysis of DNA methylation reveals a partial reprogramming of the Muller glia genome during retina regeneration. PNAS 110:4919814–19
    [Google Scholar]
  94. Qin Z, Kidd AR 3rd, Thomas JL, Poss KD, Hyde DR et al. 2011. FGF signaling regulates rod photoreceptor cell maintenance and regeneration in zebrafish. Exp. Eye Res. 93:5726–34
    [Google Scholar]
  95. Ramachandran R, Fausett BV, Goldman D 2010. Ascl1a regulates Muller glia dedifferentiation and retinal regeneration through a Lin-28-dependent, let-7 microRNA signalling pathway. Nat. Cell Biol. 12:111101–7
    [Google Scholar]
  96. Ramachandran R, Zhao XF, Goldman D 2011. Ascl1a/Dkk/beta-catenin signaling pathway is necessary and glycogen synthase kinase-3beta inhibition is sufficient for zebrafish retina regeneration. PNAS 108:3815858–63
    [Google Scholar]
  97. Ramachandran R, Zhao XF, Goldman D 2012. Insm1a-mediated gene repression is essential for the formation and differentiation of Muller glia-derived progenitors in the injured retina. Nat. Cell Biol. 14:101013–23
    [Google Scholar]
  98. Rao MB, Didiano D, Patton JG 2017. Neurotransmitter-regulated regeneration in the zebrafish retina. Stem Cell Rep 8:4831–42
    [Google Scholar]
  99. Raymond PA, Barthel LK, Bernardos RL, Perkowski JJ 2006. Molecular characterization of retinal stem cells and their niches in adult zebrafish. BMC Dev. Biol. 6:36
    [Google Scholar]
  100. Raymond PA, Reifler MJ, Rivlin PK 1988. Regeneration of goldfish retina: Rod precursors are a likely source of regenerated cells. J. Neurobiol. 19:5431–63
    [Google Scholar]
  101. Raymond PA, Rivlin PK. 1987. Germinal cells in the goldfish retina that produce rod photoreceptors. Dev. Biol. 122:1120–38
    [Google Scholar]
  102. Rehfeld F, Rohde AM, Nguyen DT, Wulczyn FG 2015. Lin28 and let-7: ancient milestones on the road from pluripotency to neurogenesis. Cell Tissue Res 359:1145–60
    [Google Scholar]
  103. Reichenbach A, Bringmann A. 2013. New functions of Muller cells. Glia 61:5651–78
    [Google Scholar]
  104. Rueda EM, Hall BM, Hill MC, Swinton PG, Tong X et al. 2019. The Hippo pathway blocks mammalian retinal Muller glial cell reprogramming. Cell Rep 27:61637–49.e6
    [Google Scholar]
  105. Sanges D, Romo N, Simonte G, Di Vicino U, Tahoces AD et al. 2013. Wnt/beta-catenin signaling triggers neuron reprogramming and regeneration in the mouse retina. Cell Rep 4:2271–86
    [Google Scholar]
  106. Sanges D, Simonte G, Di Vicino U, Romo N, Pinilla I et al. 2016. Reprogramming Muller glia via in vivo cell fusion regenerates murine photoreceptors. J. Clin. Investig. 126:83104–16
    [Google Scholar]
  107. Sawicka A, Seiser C. 2012. Histone H3 phosphorylation: a versatile chromatin modification for different occasions. Biochimie 94:112193–201
    [Google Scholar]
  108. Sharma P, Gupta S, Chaudhary M, Mitra S, Chawla B et al. 2019. Oct4 mediates Muller glia reprogramming and cell cycle exit during retina regeneration in zebrafish. Life Sci. Alliance 2:5e201900548
    [Google Scholar]
  109. Sherpa T, Fimbel SM, Mallory DE, Maaswinkel H, Spritzer SD et al. 2008. Ganglion cell regeneration following whole-retina destruction in zebrafish. Dev. Neurobiol. 68:2166–81
    [Google Scholar]
  110. Sherpa T, Hunter SS, Frey RA, Robison BD, Stenkamp DL 2011. Retinal proliferation response in the buphthalmic zebrafish, bugeye. Exp. Eye Res. 93:4424–36
    [Google Scholar]
  111. Sherpa T, Lankford T, McGinn TE, Hunter SS, Frey RA et al. 2014. Retinal regeneration is facilitated by the presence of surviving neurons. Dev. Neurobiol. 74:9851–76
    [Google Scholar]
  112. Sieger D, Moritz C, Ziegenhals T, Prykhozhij S, Peri F 2012. Long-range Ca2+ waves transmit brain-damage signals to microglia. Dev. Cell 22:61138–48
    [Google Scholar]
  113. Sifuentes CJ, Kim JW, Swaroop A, Raymond PA 2016. Rapid, dynamic activation of Muller glial stem cell responses in zebrafish. Investig. Ophthalmol. Vis. Sci. 57:135148–60
    [Google Scholar]
  114. Stenkamp DL, Satterfield R, Muhunthan K, Sherpa T, Vihtelic TS, Cameron DA 2008. Age-related cone abnormalities in zebrafish with genetic lesions in sonic hedgehog. Investig. Ophthalmol. Vis. Sci. 49:104631–40
    [Google Scholar]
  115. Subirada PV, Paz MC, Ridano ME, Lorenc VE, Vaglienti MV et al. 2018. A journey into the retina: Muller glia commanding survival and death. Eur. J. Neurosci. 47:121429–43
    [Google Scholar]
  116. Surzenko N, Crowl T, Bachleda A, Langer L, Pevny L 2013. SOX2 maintains the quiescent progenitor cell state of postnatal retinal Muller glia. Development 140:71445–56
    [Google Scholar]
  117. Takahashi K, Yamanaka S. 2006. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:4663–76
    [Google Scholar]
  118. Thomas JL, Morgan GW, Dolinski KM, Thummel R 2018. Characterization of the pleiotropic roles of Sonic Hedgehog during retinal regeneration in adult zebrafish. Exp. Eye Res. 166:106–15
    [Google Scholar]
  119. Thomas JL, Ranski AH, Morgan GW, Thummel R 2016. Reactive gliosis in the adult zebrafish retina. Exp. Eye Res. 143:98–109
    [Google Scholar]
  120. Thummel R, Burket CT, Hyde DR 2006. Two different transgenes to study gene silencing and re-expression during zebrafish caudal fin and retinal regeneration. Sci. World J. 6:Suppl. 165–81
    [Google Scholar]
  121. Todd L, Fischer AJ. 2015. Hedgehog signaling stimulates the formation of proliferating Muller glia-derived progenitor cells in the chick retina. Development 142:152610–22
    [Google Scholar]
  122. Todd L, Palazzo I, Squires N, Mendonca N, Fischer AJ 2017. BMP- and TGFbeta-signaling regulate the formation of Muller glia-derived progenitor cells in the avian retina. Glia 65:101640–55
    [Google Scholar]
  123. Todd L, Squires N, Suarez L, Fischer AJ 2016. Jak/Stat signaling regulates the proliferation and neurogenic potential of Muller glia-derived progenitor cells in the avian retina. Sci. Rep. 6:35703
    [Google Scholar]
  124. Todd L, Suarez L, Quinn C, Fischer AJ 2018. Retinoic acid-signaling regulates the proliferative and neurogenic capacity of Muller glia-derived progenitor cells in the avian retina. Stem Cells 36:3392–405
    [Google Scholar]
  125. Todd L, Volkov LI, Zelinka C, Squires N, Fischer AJ 2015. Heparin-binding EGF-like growth factor (HB-EGF) stimulates the proliferation of Muller glia-derived progenitor cells in avian and murine retinas. Mol. Cell. Neurosci. 69:54–64
    [Google Scholar]
  126. Ueki Y, Reh TA. 2013. EGF stimulates Muller glial proliferation via a BMP-dependent mechanism. Glia 61:5778–89
    [Google Scholar]
  127. Ueki Y, Wilken MS, Cox KE, Chipman L, Jorstad N et al. 2015. Transgenic expression of the proneural transcription factor Ascl1 in Muller glia stimulates retinal regeneration in young mice. PNAS 112:4413717–22
    [Google Scholar]
  128. Vecino E, Rodriguez FD, Ruzafa N, Pereiro X, Sharma SC 2016. Glia-neuron interactions in the mammalian retina. Prog. Retin. Eye Res. 51:1–40
    [Google Scholar]
  129. Veroni C, Gabriele L, Canini I, Castiello L, Coccia E et al. 2010. Activation of TNF receptor 2 in microglia promotes induction of anti-inflammatory pathways. Mol. Cell. Neurosci. 45:3234–44
    [Google Scholar]
  130. Veth KN, Willer JR, Collery RF, Gray MP, Willer GB et al. 2011. Mutations in zebrafish lrp2 result in adult-onset ocular pathogenesis that models myopia and other risk factors for glaucoma. PLOS Genet 7:2e1001310
    [Google Scholar]
  131. Vetter ML, Moore KB. 2001. Becoming glial in the neural retina. Dev. Dyn. 221:2146–53
    [Google Scholar]
  132. Vihtelic TS, Hyde DR. 2000. Light-induced rod and cone cell death and regeneration in the adult albino zebrafish (Danio rerio) retina. J. Neurobiol. 44:3289–307
    [Google Scholar]
  133. Voigt P, Tee WW, Reinberg D 2013. A double take on bivalent promoters. Genes Dev 27:121318–38
    [Google Scholar]
  134. Wan J, Goldman D. 2017. Opposing actions of Fgf8a on Notch signaling distinguish two Muller glial cell populations that contribute to retina growth and regeneration. Cell Rep 19:4849–62
    [Google Scholar]
  135. Wan J, Ramachandran R, Goldman D 2012. HB-EGF is necessary and sufficient for Muller glia dedifferentiation and retina regeneration. Dev. Cell 22:2334–47
    [Google Scholar]
  136. Wan J, Zhao XF, Vojtek A, Goldman D 2014. Retinal injury, growth factors, and cytokines converge on beta-catenin and pStat3 signaling to stimulate retina regeneration. Cell Rep 9:1285–97
    [Google Scholar]
  137. White DT, Sengupta S, Saxena MT, Xu Q, Hanes J et al. 2017. Immunomodulation-accelerated neuronal regeneration following selective rod photoreceptor cell ablation in the zebrafish retina. PNAS 114:18E3719–28
    [Google Scholar]
  138. Willkomm L, Bloch W. 2015. State of the art in cell-cell fusion. Methods Mol. Biol. 1313:1–19
    [Google Scholar]
  139. Wu DM, Schneiderman T, Burgett J, Gokhale P, Barthel L, Raymond PA 2001. Cones regenerate from retinal stem cells sequestered in the inner nuclear layer of adult goldfish retina. Investig. Ophthalmol. Vis. Sci. 42:92115–24
    [Google Scholar]
  140. Yao K, Qiu S, Tian L, Snider WD, Flannery JG et al. 2016. Wnt regulates proliferation and neurogenic potential of Muller glial cells via a Lin28/let-7 miRNA-dependent pathway in adult mammalian retinas. Cell Rep 17:1165–78
    [Google Scholar]
  141. Yin M, Chen Z, Ouyang Y, Zhang H, Wan Z et al. 2017. Thrombin-induced, TNFR-dependent miR-181c downregulation promotes MLL1 and NF-κB target gene expression in human microglia. J. Neuro-inflamm. 14:1132
    [Google Scholar]
  142. Yoshimatsu T, D'Orazi FD, Gamlin CR, Suzuki SC, Suli A et al. 2016. Presynaptic partner selection during retinal circuit reassembly varies with timing of neuronal regeneration in vivo. Nat. Commun. 7:10590
    [Google Scholar]
  143. Yurco P, Cameron DA. 2005. Responses of Muller glia to retinal injury in adult zebrafish. Vis. Res. 45:8991–1002
    [Google Scholar]
  144. Yurco P, Cameron DA. 2007. Cellular correlates of proneural and Notch-delta gene expression in the regenerating zebrafish retina. Vis. Neurosci. 24:3437–43
    [Google Scholar]
  145. Zelinka CP, Volkov L, Goodman ZA, Todd L, Palazzo I et al. 2016. mTor signaling is required for the formation of proliferating Muller glia-derived progenitor cells in the chick retina. Development 143:111859–73
    [Google Scholar]
  146. Zhang S, Bell E, Zhi H, Brown S, Imran SAM et al. 2019. OCT4 and PAX6 determine the dual function of SOX2 in human ESCs as a key pluripotent or neural factor. Stem Cell Res. Therapy 10:1122
    [Google Scholar]
  147. Zhao XF, Wan J, Powell C, Ramachandran R, Myers MG Jr, Goldman D 2014. Leptin and IL-6 family cytokines synergize to stimulate Muller glia reprogramming and retina regeneration. Cell Rep 9:1272–84
    [Google Scholar]
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