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Turning Müller Glia into Neural Progenitors in the Retina

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Abstract

Stimulating neuronal regeneration is a potential strategy to treat sight-threatening diseases of the retina. In some classes of vertebrates, retinal regeneration occurs spontaneously to effectively replace neurons lost to acute damage in order to restore visual function. There are different mechanisms and cellular sources of retinal regeneration in different species, include the retinal pigmented epithelium, progenitors seeded across the retina, and the Müller glia. This review briefly summarizes the different mechanisms of retinal regeneration in frogs, fish, chicks, and rodents. The bulk of this review summarizes and discusses recent findings regarding regeneration from Müller glia-derived progenitors, with emphasis on findings in the chick retina. The Müller glia are a promising source of regeneration-supporting cells that are intrinsic to the retina and significant evidence indicated these glias can be stimulated to produce neurons in different classes of vertebrates. The key to harnessing the neurogenic potential of Müller glia is to identify the secreted factors, signaling pathways, and transcription factors that enable de-differentiation, proliferation, and neurogenesis. We review findings regarding the roles of mitogen-activated protein kinase and notch signaling in the proliferation and generation of Müller glia-derived retinal progenitors.

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References

  1. Stone L (1950) Neural retina degeneration followed by regeneration from surviving pigment cells in grafted adult salamander eyes. Anat Rec 106:89–110

    Article  PubMed  CAS  Google Scholar 

  2. Stone L (1950) The role of retinal pigment cells in regenerating neural retinae of adult salamander eyes. J Exp Zool 113:9–31

    Article  Google Scholar 

  3. Akimenko MA, Mari-Beffa M, Becerra J, Geraudie J (2003) Old questions, new tools, and some answers to the mystery of fin regeneration. Dev Dyn 226:190–201

    Article  PubMed  Google Scholar 

  4. Poss KD, Wilson LG, Keating MT (2002) Heart regeneration in zebrafish. Science 298:2188–2190

    Article  PubMed  CAS  Google Scholar 

  5. Becker CG, Becker T (2008) Adult zebrafish as a model for successful central nervous system regeneration. Restor Neurol Neurosci 26:71–80

    PubMed  Google Scholar 

  6. Bernhardt RR, Tongiorgi E, Anzini P, Schachner M (1996) Increased expression of specific recognition molecules by retinal ganglion cells and by optic pathway glia accompanies the successful regeneration of retinal axons in adult zebrafish. J Comp Neurol 376:253–264

    Article  PubMed  CAS  Google Scholar 

  7. Vihtelic TS, Hyde DR (2000) Light-induced rod and cone cell death and regeneration in the adult albino zebrafish (Danio rerio) retina. J Neurobiol 44:289–307

    Article  PubMed  CAS  Google Scholar 

  8. Hitchcock P, Ochocinska M, Sieh A, Otteson D (2004) Persistent and injury-induced neurogenesis in the vertebrate retina. Prog Retin Eye Res 23:183–194

    Article  PubMed  Google Scholar 

  9. Hitchcock PF, Raymond PA (1992) Retinal regeneration. Trends Neurosci 15:103–108

    Article  PubMed  CAS  Google Scholar 

  10. Raymond PA, Hitchcock PF (2000) How the neural retina regenerates. Results Probl Cell Differ 31:197–218

    PubMed  CAS  Google Scholar 

  11. 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 518:800–14

    Article  PubMed  CAS  Google Scholar 

  12. 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 27:7028–7040

    Article  PubMed  CAS  Google Scholar 

  13. Fausett BV, Goldman D (2006) A role for alpha1 tubulin-expressing Muller glia in regeneration of the injured zebrafish retina. J Neurosci 26:6303–6313

    Article  PubMed  CAS  Google Scholar 

  14. Qin Z, Barthel LK, Raymond PA (2009) Genetic evidence for shared mechanisms of epimorphic regeneration in zebrafish. Proc Natl Acad Sci USA 106:9310–9315

    Article  PubMed  Google Scholar 

  15. Stenkamp DL, Powers MK, Carney LH, Cameron DA (2001) Evidence for two distinct mechanisms of neurogenesis and cellular pattern formation in regenerated goldfish retinas. J Comp Neurol 431:363–381

    Article  PubMed  CAS  Google Scholar 

  16. Becker CG, Becker T (2007) Growth and pathfinding of regenerating axons in the optic projection of adult fish. J Neurosci Res 85:2793–2799

    Article  PubMed  CAS  Google Scholar 

  17. Stenkamp DL (2007) Neurogenesis in the fish retina. Int Rev Cytol 259:173–224

    Article  PubMed  CAS  Google Scholar 

  18. Yokoyama H (2008) Initiation of limb regeneration: the critical steps for regenerative capacity. Dev Growth Differ 50:13–22

    Article  PubMed  CAS  Google Scholar 

  19. Kurosaka H, Takano-Yamamoto T, Yamashiro T, Agata K (2008) Comparison of molecular and cellular events during lower jaw regeneration of newt (Cynops pyrrhogaster) and West African clawed frog (Xenopus tropicalis). Dev Dyn 237:354–365

    Article  PubMed  CAS  Google Scholar 

  20. Singh BN, Koyano-Nakagawa N, Garry JP, Weaver CV (2010) Heart of newt: a recipe for regeneration. J Cardiovasc Transl Res 3:397–409

    Article  PubMed  Google Scholar 

  21. Mitsuda S, Yoshii C, Ikegami Y, Araki M (2005) Tissue interaction between the retinal pigment epithelium and the choroid triggers retinal regeneration of the newt Cynops pyrrhogaster. Dev Biol 280:122–132

    Article  PubMed  CAS  Google Scholar 

  22. Mizuno N, Mochii M, Yamamoto TS, Takahashi TC, Eguchi G, Okada TS (1999) Pax-6 and Prox 1 expression during lens regeneration from Cynops iris and Xenopus cornea: evidence for a genetic program common to embryonic lens development. Differentiation 65:141–149

    Article  PubMed  CAS  Google Scholar 

  23. Margotta V, Filoni S, Merante A, Chimenti C (2002) Analysis of morphogenetic potential of caudal spinal cord in Triturus carnifex adults (Urodele amphibians) subjected to repeated tail amputations. Ital J Anat Embryol 107:127–144

    PubMed  Google Scholar 

  24. Stroeva OG, Mitashov VI (1983) Retinal pigment epithelium: proliferation and differentiation during development and regeneration. Int Rev Cytol 83:221–293

    Article  PubMed  CAS  Google Scholar 

  25. Okada TS (1980) Cellular metaplasia or transdifferentiation as a model for retinal cell differentiation. Curr Top Dev Biol 16:349–380

    Article  PubMed  CAS  Google Scholar 

  26. Negishi K, Shinagawa S (1993) Fibroblast growth factor induces proliferating cell nuclear antigen-immunoreactive cells in goldfish retina. Neurosci Res 18:143–56

    Google Scholar 

  27. Reh TA (1987) Cell-specific regulation of neuronal production in the larval frog retina. J Neurosci 7:3317–3324

    PubMed  CAS  Google Scholar 

  28. Reh TA, Nagy T, Gretton H (1987) Retinal pigmented epithelial cells induced to transdifferentiate to neurons by laminin. Nature 330:68–71

    Article  PubMed  CAS  Google Scholar 

  29. Araki M (2007) Regeneration of the amphibian retina: role of tissue interaction and related signaling molecules on RPE transdifferentiation. Dev Growth Differ 49:109–120

    Article  PubMed  Google Scholar 

  30. Reh TA, Jones M, Pittack C (1991) Common mechanisms of retinal regeneration in the larval frog and embryonic chick. Ciba Found Symp 160:192–204, discussion 204–8

    PubMed  CAS  Google Scholar 

  31. Sakaguchi DS, Janick LM, Reh TA (1997) Basic fibroblast growth factor (FGF-2) induced transdifferentiation of retinal pigment epithelium: generation of retinal neurons and glia. Dev Dyn 209:387–398

    Article  PubMed  CAS  Google Scholar 

  32. Park CM, Hollenberg MJ (1989) Basic fibroblast growth factor induces retinal regeneration in vivo. Dev Biol 134:201–205

    Article  PubMed  CAS  Google Scholar 

  33. Park CM, Hollenberg MJ (1991) Induction of retinal regeneration in vivo by growth factors. Dev Biol 148:322–333

    Article  PubMed  CAS  Google Scholar 

  34. Pittack C, Jones M, Reh TA (1991) Basic fibroblast growth factor induces retinal pigment epithelium to generate neural retina in vitro. Development 113:577–588

    PubMed  CAS  Google Scholar 

  35. Zhao S, Thornquist SC, Barnstable CJ (1995) In vitro transdifferentiation of embryonic rat retinal pigment epithelium to neural retina. Brain Res 677:300–310

    Article  PubMed  CAS  Google Scholar 

  36. Coulombre JL, Coulombre AJ (1965) Regeneration of neural retina from the pigmented epithelium in the chick embryo. Dev Biol 12:79–92

    Article  PubMed  CAS  Google Scholar 

  37. Park CM, Hollenberg MJ (1993) Growth factor-induced retinal regeneration in vivo. Int Rev Cytol 146:49–74

    Article  PubMed  CAS  Google Scholar 

  38. Vogel-Hopker A, Momose T, Rohrer H, Yasuda K, Ishihara L, Rapaport DH (2000) Multiple functions of fibroblast growth factor-8 (FGF-8) in chick eye development. Mech Dev 94:25–36

    Article  PubMed  CAS  Google Scholar 

  39. Haynes T, Gutierrez C, Aycinena JC, Tsonis PA, Del Rio-Tsonis K (2007) BMP signaling mediates stem/progenitor cell-induced retina regeneration. Proc Natl Acad Sci USA 104:20380–20385

    PubMed  CAS  Google Scholar 

  40. Spence JR, Aycinena JC, Del Rio-Tsonis K (2007) Fibroblast growth factor-hedgehog interdependence during retina regeneration. Dev Dyn 236:1161–1174

    Article  PubMed  CAS  Google Scholar 

  41. Spence JR, Madhavan M, Ewing JD, Jones DK, Lehman BM, Del Rio-Tsonis K (2004) The hedgehog pathway is a modulator of retina regeneration. Development 131:4607–4621

    Article  PubMed  CAS  Google Scholar 

  42. Wang SZ, Ma W, Yan RT, Mao W (2010) Generating retinal neurons by reprogramming retinal pigment epithelial cells. Expert Opin Biol Ther 10:1227–1239

    Article  PubMed  CAS  Google Scholar 

  43. Fischer AJ, Reh TA (2001) Transdifferentiation of pigmented epithelial cells: a source of retinal stem cells? Dev Neurosci 23:268–276

    Article  PubMed  CAS  Google Scholar 

  44. Fischer AJ, Reh TA (2000) Identification of a proliferating marginal zone of retinal progenitors in postnatal chickens. Dev Biol 220:197–210

    Article  PubMed  CAS  Google Scholar 

  45. Kubota R, Hokoc JN, Moshiri A, McGuire C, Reh TA (2002) A comparative study of neurogenesis in the retinal ciliary marginal zone of homeothermic vertebrates. Brain Res Dev Brain Res 134:31–41

    Article  PubMed  CAS  Google Scholar 

  46. Fischer AJ (2005) Neural regeneration in the chick retina. Prog Retin Eye Res 24:161–182

    Article  PubMed  Google Scholar 

  47. Fischer AJ, Reh TA (2003) Growth factors induce neurogenesis in the ciliary body. Dev Biol 259:225–240

    Article  PubMed  CAS  Google Scholar 

  48. Tropepe V, Coles BL, Chiasson BJ, Horsford DJ, Elia AJ, McInnes RR, van der Kooy D (2000) Retinal stem cells in the adult mammalian eye. Science 287:2032–2036

    Article  PubMed  CAS  Google Scholar 

  49. Cicero SA, Johnson D, Reyntjens S, Frase S, Connell S, Chow LM, Baker SJ, Sorrentino BP, Dyer MA (2009) Cells previously identified as retinal stem cells are pigmented ciliary epithelial cells. Proc Natl Acad Sci USA 106:6685–6690

    Article  PubMed  Google Scholar 

  50. Gualdoni S, Baron M, Lakowski J, Decembrini S, Smith AJ, Pearson RA, Ali RR, Sowden JC (2010) Adult ciliary epithelial cells, previously identified as retinal stem cells with potential for retinal repair, fail to differentiate into new rod photoreceptors. Stem Cells 28:1048–1059

    Article  PubMed  CAS  Google Scholar 

  51. Moshiri A, Reh TA (2004) Persistent progenitors at the retinal margin of ptc+/−mice. J Neurosci 24:229–237

    Article  PubMed  CAS  Google Scholar 

  52. Fischer AJ, Scott MA, Zelinka C, Sherwood P (2010) A novel type of glial cell in the retina is stimulated by insulin-like growth factor 1 and may exacerbate damage to neurons and Muller glia. Glia 58:633–649

    Article  PubMed  Google Scholar 

  53. Rompani SB, Cepko CL (2010) A common progenitor for retinal astrocytes and oligodendrocytes. J Neurosci 30:4970–4980

    Article  PubMed  CAS  Google Scholar 

  54. Fischer AJ, Reh TA (2001) Muller glia are a potential source of neural regeneration in the postnatal chicken retina. Nat Neurosci 4:247–252

    Article  PubMed  CAS  Google Scholar 

  55. Karl MO, Hayes S, Nelson BR, Tan K, Buckingham B, Reh TA (2008) Stimulation of neural regeneration in the mouse retina. Proc Natl Acad Sci USA 105:19508–19513

    Article  PubMed  Google Scholar 

  56. Ooto S, Akagi T, Kageyama R, Akita J, Mandai M, Honda Y, Takahashi M (2004) Potential for neural regeneration after neurotoxic injury in the adult mammalian retina. Proc Natl Acad Sci USA 101:13654–13659

    Article  PubMed  CAS  Google Scholar 

  57. Fischer AJ, McGuire CR, Dierks BD, Reh TA (2002) Insulin and fibroblast growth factor 2 activate a neurogenic program in Muller glia of the chicken retina. J Neurosci 22:9387–9398

    PubMed  CAS  Google Scholar 

  58. Fischer AJ, Scott MA, Tuten W (2009) Mitogen-activated protein kinase-signaling stimulates Muller glia to proliferate in acutely damaged chicken retina. Glia 57:166–181

    Article  PubMed  Google Scholar 

  59. Hayes S, Nelson BR, Buckingham B, Reh TA (2007) Notch signaling regulates regeneration in the avian retina. Dev Biol 312:300–311

    Article  PubMed  CAS  Google Scholar 

  60. Fischer AJ, Scott MA, Ritchey ER, Sherwood P (2009) Mitogen-activated protein kinase-signaling regulates the ability of Muller glia to proliferate and protect retinal neurons against excitotoxicity. Glia 57:1538–1552

    Article  PubMed  Google Scholar 

  61. Thummel R, Enright JM, Kassen SC, Montgomery JE, Bailey TJ, Hyde DR (2010) Pax6a and Pax6b are required at different points in neuronal progenitor cell proliferation during zebrafish photoreceptor regeneration. Exp Eye Res 90:572–582

    Article  PubMed  CAS  Google Scholar 

  62. Fausett BV, Gumerson JD, Goldman D (2008) The proneural basic helix-loop-helix gene ascl1a is required for retina regeneration. J Neurosci 28:1109–1117

    Article  PubMed  CAS  Google Scholar 

  63. Bernardos RL, Lentz SI, Wolfe MS, Raymond PA (2005) Notch-Delta signaling is required for spatial patterning and Muller glia differentiation in the zebrafish retina. Dev Biol 278:381–395

    Article  PubMed  CAS  Google Scholar 

  64. 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

    Article  PubMed  CAS  Google Scholar 

  65. Fischer AJ, Omar G (2005) Transitin, a nestin-related intermediate filament, is expressed by neural progenitors and can be induced in Muller glia in the chicken retina. J Comp Neurol 484:1–14

    Article  PubMed  CAS  Google Scholar 

  66. Reh TA, Fischer AJ (2001) Stem cells in the vertebrate retina. Brain Behav Evol 58:296–305

    Article  PubMed  CAS  Google Scholar 

  67. Fischer AJ, Reh TA (2003) Potential of Muller glia to become neurogenic retinal progenitor cells. Glia 43:70–76

    Article  PubMed  Google Scholar 

  68. Yurco P, Cameron DA (2005) Responses of Muller glia to retinal injury in adult zebrafish. Vis Res 45:991–1002

    Article  PubMed  Google Scholar 

  69. Lawrence JM, Singhal S, Bhatia B, Keegan DJ, Reh TA, Luthert PJ, Khaw PT, Limb GA (2007) MIO-M1 cells and similar muller glial cell lines derived from adult human retina exhibit neural stem cell characteristics. Stem Cells 25:2033–2043

    Article  PubMed  CAS  Google Scholar 

  70. Fischer AJ, Wang SZ, Reh TA (2004) NeuroD induces the expression of visinin and calretinin by proliferating cells derived from toxin-damaged chicken retina. Dev Dyn 229:555–563

    Article  PubMed  CAS  Google Scholar 

  71. Fischer AJ, Schmidt M, Omar G, Reh TA (2004) BMP4 and CNTF are neuroprotective and suppress damage-induced proliferation of Muller glia in the retina. Mol Cell Neurosci 27:531–542

    Article  PubMed  CAS  Google Scholar 

  72. Stuermer CA, Easter SS, Jr (1984) A comparison of the normal and regenerated retinotectal pathways of goldfish. J Comp Neurol 223:57–76

    Google Scholar 

  73. Hitchcock PF, Cirenza P (1994) Synaptic organization of regenerated retina in the goldfish. J Comp Neurol 343:609–616

    Google Scholar 

  74. Fimbel SM, Montgomery JE, Burket CT, Hyde DR (2007) Regeneration of inner retinal neurons after intravitreal injection of ouabain in zebrafish. J Neurosci 27:1712–1724

    Article  PubMed  CAS  Google Scholar 

  75. Lindsey AE, Powers MK (2007) Visual behavior of adult goldfish with regenerating retina. Vis Neurosci 24:247–255

    Article  PubMed  Google Scholar 

  76. Mensinger AF, Powers MK (1999) Visual function in regenerating teleost retina following cytotoxic lesioning. Vis Neurosci 16:241–251

    Article  PubMed  CAS  Google Scholar 

  77. Mensinger AF, Powers MK (2007) Visual function in regenerating teleost retina following surgical lesioning. Vis Neurosci 24:299–307

    Article  PubMed  Google Scholar 

  78. Sherpa T, Fimbel SM, Mallory DE, Maaswinkel H, Spritzer SD, Sand JA, Li L, Hyde DR, Stenkamp DL (2008) Ganglion cell regeneration following whole-retina destruction in zebrafish. Dev Neurobiol 68:166–181

    Article  PubMed  Google Scholar 

  79. 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 68:605–619

    Article  PubMed  Google Scholar 

  80. 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 88:1051–1064

    Article  PubMed  CAS  Google Scholar 

  81. Kirsch M, Lee MY, Meyer V, Wiese A, Hofmann HD (1997) Evidence for multiple, local functions of ciliary neurotrophic factor (CNTF) in retinal development: expression of CNTF and its receptors and in vitro effects on target cells. J Neurochem 68:979–990

    Article  PubMed  CAS  Google Scholar 

  82. Peterson WM, Wang Q, Tzekova R, Wiegand SJ (2000) Ciliary neurotrophic factor and stress stimuli activate the Jak-STAT pathway in retinal neurons and glia. J Neurosci 20:4081–4090

    PubMed  CAS  Google Scholar 

  83. Wahlin KJ, Campochiaro PA, Zack DJ, Adler R (2000) Neurotrophic factors cause activation of intracellular signaling pathways in Muller cells and other cells of the inner retina, but not photoreceptors. Invest Ophthalmol Vis Sci 41:927–936

    PubMed  CAS  Google Scholar 

  84. Wang Y, Smith SB, Ogilvie JM, McCool DJ, Sarthy V (2002) Ciliary neurotrophic factor induces glial fibrillary acidic protein in retinal Muller cells through the JAK/STAT signal transduction pathway. Curr Eye Res 24:305–312

    Article  PubMed  CAS  Google Scholar 

  85. Fischer AJ, Omar G, Eubanks J, McGuire CR, Dierks BD, Reh TA (2004) Different aspects of gliosis in retinal Müller glia can be induced by CNTF, insulin and FGF2 in the absence of damage. Mol Vision 10:973–986

    CAS  Google Scholar 

  86. Stanke JJ, Moose H, El-Hodiri HM, Fischer AJ (2010) A comparative study of Pax2 expression in glial cells in the retinas of birds and mammals. J Comp Neurol 518:2316–2333

    Article  PubMed  CAS  Google Scholar 

  87. Lewis GP, Fisher SK (2003) Up-regulation of glial fibrillary acidic protein in response to retinal injury: its potential role in glial remodeling and a comparison to vimentin expression. Int Rev Cytol 230:263–290

    Article  PubMed  CAS  Google Scholar 

  88. Fischer AJ, Zelinka C, Scott MA (2010) Heterogeneity of glia in the retina and optic nerve of birds and mammals. PLoS ONE 5:e10774

    Article  PubMed  CAS  Google Scholar 

  89. Boije H, Ring H, Lopez-Gallardo M, Prada C, Hallbook F (2010) Pax2 is expressed in a subpopulation of Muller cells in the central chick retina. Dev Dyn 239:1858–1866

    Article  PubMed  CAS  Google Scholar 

  90. Schulte D, Furukawa T, Peters MA, Kozak CA, Cepko CL (1999) Misexpression of the Emx-related homeobox genes cVax and mVax2 ventralizes the retina and perturbs the retinotectal map. Neuron 24:541–553

    Article  PubMed  CAS  Google Scholar 

  91. Sehgal R, Karcavich R, Carlson S, Belecky-Adams TL (2008) Ectopic Pax2 expression in chick ventral optic cup phenocopies loss of Pax2 expression. Dev Biol 319:23–33

    Article  PubMed  CAS  Google Scholar 

  92. Washbourne P, McAllister AK (2002) Techniques for gene transfer into neurons. Curr Opin Neurobiol 12:566–573

    Article  PubMed  CAS  Google Scholar 

  93. Marquardt T (2003) Transcriptional control of neuronal diversification in the retina. Prog Retin Eye Res 22:567–577

    Article  PubMed  CAS  Google Scholar 

  94. Sullivan SA, Barthel LK, Largent BL, Raymond PA (1997) A goldfish notch-3 homologue is expressed in neurogenic regions of embryonic, adult, and regenerating brain and retina. Dev Genet 20:208–223

    Article  PubMed  CAS  Google Scholar 

  95. Dorsky RI, Chang WS, Rapaport DH, Harris WA (1997) Regulation of neuronal diversity in the Xenopus retina by Delta signalling. Nature 385:67–70

    Article  PubMed  CAS  Google Scholar 

  96. Dorsky RI, Rapaport DH, Harris WA (1995) Xotch inhibits cell differentiation in the Xenopus retina. Neuron 14:487–496

    Article  PubMed  CAS  Google Scholar 

  97. 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 26:383–394

    Article  PubMed  CAS  Google Scholar 

  98. Ghai K, Zelinka C, Fischer AJ (2010) Notch signaling influences the neuroprotective and proliferative properties of Müller glia. J Neurosci 30:3101–3112

    Article  PubMed  CAS  Google Scholar 

  99. Stanke JJ, Fischer AJ (2010) Embryonic retinal progenitors provide trophic support to mature retinal neurons. Invest Ophthalmol Vis Sci 51:2208–2218

    Article  PubMed  Google Scholar 

  100. Close JL, Gumuscu B, Reh TA (2005) Retinal neurons regulate proliferation of postnatal progenitors and Muller glia in the rat retina via TGF beta signaling. Development 132:3015–3026

    Article  PubMed  CAS  Google Scholar 

  101. Osakada F, Ooto S, Akagi T, Mandai M, Akaike A, Takahashi M (2007) Wnt signaling promotes regeneration in the retina of adult mammals. J Neurosci 27:4210–4219

    Article  PubMed  CAS  Google Scholar 

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Fischer, A.J., Bongini, R. Turning Müller Glia into Neural Progenitors in the Retina. Mol Neurobiol 42, 199–209 (2010). https://doi.org/10.1007/s12035-010-8152-2

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