Skip to main content

The Regenerative Potential of the Vertebrate Retina: Lessons from the Zebrafish

  • Chapter
  • First Online:
Regenerative Biology of the Eye

Part of the book series: Stem Cell Biology and Regenerative Medicine ((STEMCELL))

Abstract

The regenerative potential, forward/reverse genetic capabilities and technical advantages of the zebrafish make it an ideal model for studying signals and mechanisms that drive retinal regeneration. Here, we describe the different cellular sources of regeneration in zebrafish, with a particular emphasis on Müller glia cells, as well as the individual signalling pathways that specifically co-ordinate the different phases of regeneration. Because the same cells are also generated developmentally, a comparison between developmental and regenerative processes is of particular benefit to identify the extent to which we can drive developmental mechanisms to improve adult regenerative responses. Given the recent identification of many conserved signalling pathways using zebrafish developmental studies, we can now use this model system to assess their involvement during regeneration. Finally, identifying similarities and differences between zebrafish and amniotic vertebrates allows us to distinguish between the intrinsic capacity and extrinsic signals that can improve regeneration. Thus, we aim to highlight data obtained from the zebrafish vertebrate model and how this information can and has contributed to and directed mammalian research.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

ADP:

Adenosine diphosphate

Ascl1a:

Achaete-scute complex like 1a

Atoh7:

Atonal homolog 7

ATP:

Adenosine triphosphate

bHLH:

Basic helix loop helix

Bmp:

Bone morphogenetic protein

Brn3b:

Brain-specific homeobox 3b

CGZ:

Circumferential germinal zone

Chx10:

Ceh-10 homeodomain containing homolog

CMZ:

Ciliary margin zone

CNTF:

Ciliary neurotrophic factor

Crx:

Cone rod homeobox

Dkk1b:

Dickkopf 1b

Dll1:

Delta-like 1

Dpi:

Days post-injury

Drgal1-L2:

β-Galactoside-binding protein galectin 1-like 2

ERG:

Electroretinogram

Fgf8:

Fibroblast growth factor 8

FoxN4:

Forkhead box N4

Fzd2:

Frizzled 2

Gap43:

Growth-associated protein 43

GCL:

Ganglion cell layer

GFAP:

Glial fibrillary acidic protein

GSK-3β:

Glycogen synthase kinase-3β

HB-EGF:

Heparin-binding epidermal like growth factor

Hes5:

Hairy and enhancer of split 5

Hpi:

Hours post-injury

Hspd1:

Heat shock 60-kDa protein 1

Id2a:

Inhibitory of differentiation 2

IgF:

Insulin growth factor

IKNM:

Interkinetic nuclear migration

INL:

Inner nuclear layer

Insm1a:

Insulinoma-associated 1a

MAPK:

Mitogen-activated protein kinase

Mcm:

Minichromosome maintenance protein

Mps1:

Monopolar spindle 1

Ngn1:

Neurogenin 1

NMDA:

N-methyl-d-aspartate

Oct4:

Octamer-binding transcription factor 4

Olig2:

Oligodendrocyte transcription factor 2

ONL:

Outer nuclear layer

Pax6:

Paired box 6

PCNA:

Proliferating cell nuclear antigen

PDGFA:

Platelet-derived growth factor A

Rac1:

Ras-related C3 botulinum toxin substrate 1

Shh/Hh:

Sonic hedgehog/Hedgehog

Six3b:

Sine-oculis homeobox homolog 3b

Sox2:

Sex determining region Y-box 2

Stat3:

Signal transducer and activator of transcription 3

TGFβ:

Transforming growth factor beta

Tgif1:

Transforming growth interacting factor

TNFα:

Tumour necrosis factor alpha

Trb:

Thyroid hormone receptor β

Tuba1a/α1T:

α1-Tubulin

UAS:

Upstream activating sequence

Vsx1/Vsx2:

Visual homeobox transcription factors 1 and 2

References

  1. Tanaka EM, Reddien PW (2011) The cellular basis for animal regeneration. Dev Cell 21(1):172–185

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  2. Knapp D, Tanaka EM (2012) Regeneration and reprogramming. Curr Opin Genet Dev 22(5):485–493

    Article  CAS  PubMed  Google Scholar 

  3. Karl MO, Reh TA (2010) Regenerative medicine for retinal diseases: activating endogenous repair mechanisms. Trends Mol Med 16(4):193–202

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  4. Gemberling M, Bailey TJ, Hyde DR, Poss KD (2013) The zebrafish as a model for complex tissue regeneration. Trends Genet 29(11):611–620

    Google Scholar 

  5. McMahon DG (1994) Modulation of electrical synaptic transmission in zebrafish retinal horizontal cells. J Neurosci 14(3 pt 2):1722–1734

    CAS  PubMed  Google Scholar 

  6. Raymond PA, Barthel LK, Rounsifer ME, Sullivan SA, Knight JK (1993) Expression of rod and cone visual pigments in goldfish and zebrafish: a rhodopsin-like gene is expressed in cones. Neuron 10(6):1161–1174

    Article  CAS  PubMed  Google Scholar 

  7. Jusuf PR, Harris WA (2009) Ptf1a is expressed transiently in all types of amacrine cells in the embryonic zebrafish retina. Neural Dev 4:34

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  8. Jusuf PR et al (2011) Origin and determination of inhibitory cell lineages in the vertebrate retina. J Neurosci 31(7):2549–2562

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  9. Wassle H, Puller C, Muller F, Haverkamp S (2009) Cone contacts, mosaics, and territories of bipolar cells in the mouse retina. J Neurosci 29(1):106–117

    Article  PubMed  CAS  Google Scholar 

  10. Mangrum WI, Dowling JE, Cohen ED (2002) A morphological classification of ganglion cells in the zebrafish retina. Vis Neurosci 19(6):767–779

    Article  PubMed  Google Scholar 

  11. Stiemke MM, Hollyfield JG (1995) Cell birthdays in Xenopus laevis retina. Differentiation 58(3):189–193

    Article  CAS  PubMed  Google Scholar 

  12. Rapaport DH, Wong LL, Wood ED, Yasumura D, LaVail MM (2004) Timing and topography of cell genesis in the rat retina. J Comp Neurol 474(2):304–324

    Article  PubMed  Google Scholar 

  13. La Vail MM, Rapaport DH, Rakic P (1991) Cytogenesis in the monkey retina. J Comp Neurol 309(1):86–114

    Article  PubMed  Google Scholar 

  14. Nawrocki L, BreMiller R, Streisinger G, Kaplan M (1985) Larval and adult visual pigments of the zebrafish, Brachydanio rerio. Vision Res 25(11):1569–1576

    Article  CAS  PubMed  Google Scholar 

  15. Hollyfield JG (1972) Histogenesis of the retina in the killifish, Fundulus heteroclitus. J Comp Neurol 144(3):373–380

    Article  CAS  PubMed  Google Scholar 

  16. Sharma SC, Ungar F (1980) Histogenesis of the goldfish retina. J Comp Neurol 191(3):373–382

    Article  CAS  PubMed  Google Scholar 

  17. Fujita S, Horii M (1963) Analysis of cytogenesis in chick retina by tritiated thymidine autoradiography. Arch Histol Jpn 23:359–366

    Article  CAS  PubMed  Google Scholar 

  18. Harada T, Harada C, Parada LF (2007) Molecular regulation of visual system development: more than meets the eye. Genes Dev 21(4):367–378

    Article  CAS  PubMed  Google Scholar 

  19. Ohsawa R, Kageyama R (2008) Regulation of retinal cell fate specification by multiple transcription factors. Brain Res 1192:90–98

    Article  CAS  PubMed  Google Scholar 

  20. Hatakeyama J, Kageyama R (2004) Retinal cell fate determination and bHLH factors. Semin Cell Dev Biol 15(1):83–89

    Article  CAS  PubMed  Google Scholar 

  21. Agathocleous M, Harris WA (2006) Cell determination. In: Sernagor E, Eglen S, Harris WA, Wong RO (eds) Retinal development. Cambridge University Press, New York, pp 75–98

    Chapter  Google Scholar 

  22. Burmeister M et al (1996) Ocular retardation mouse caused by Chx10 homeobox null allele: impaired retinal progenitor proliferation and bipolar cell differentiation. Nat Genet 12(4):376–384

    Article  CAS  PubMed  Google Scholar 

  23. Brown NL, Patel S, Brzezinski J, Glaser T (2001) Math5 is required for retinal ganglion cell and optic nerve formation. Development 128(13):2497–2508

    CAS  PubMed Central  PubMed  Google Scholar 

  24. Nakhai H et al (2007) Ptf1a is essential for the differentiation of GABAergic and glycinergic amacrine cells and horizontal cells in the mouse retina. Development 134(6):1151–1160

    Article  CAS  PubMed  Google Scholar 

  25. Hatakeyama J, Tomita K, Inoue T, Kageyama R (2001) Roles of homeobox and bHLH genes in specification of a retinal cell type. Development 128(8):1313–1322

    CAS  PubMed  Google Scholar 

  26. Vitorino M et al (2009) Vsx2 in the zebrafish retina: restricted lineages through derepression. Neural Dev 4:14

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  27. Barabino SM, Spada F, Cotelli F, Boncinelli E (1997) Inactivation of the zebrafish homologue of Chx10 by antisense oligonucleotides causes eye malformations similar to the ocular retardation phenotype. Mech Dev 63(2):133–143

    Article  CAS  PubMed  Google Scholar 

  28. Kay JN, Finger-Baier KC, Roeser T, Staub W, Baier H (2001) Retinal ganglion cell genesis requires lakritz, a Zebrafish atonal Homolog. Neuron 30(3):725–736

    Article  CAS  PubMed  Google Scholar 

  29. Dong PD, Provost E, Leach SD, Stainier DY (2008) Graded levels of Ptf1a differentially regulate endocrine and exocrine fates in the developing pancreas. Genes Dev 22(11):1445–1450

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  30. Reis LM et al (2011) VSX2 mutations in autosomal recessive microphthalmia. Mol Vis 17:2527–2532

    CAS  PubMed Central  PubMed  Google Scholar 

  31. Prasov L et al (2012) ATOH7 mutations cause autosomal recessive persistent hyperplasia of the primary vitreous. Hum Mol Genet 21(16):3681–3694

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  32. Gonzalez-Cordero A et al (2013) Photoreceptor precursors derived from three-dimensional embryonic stem cell cultures integrate and mature within adult degenerate retina. Nat Biotechnol 31(8):741–747

    Article  CAS  PubMed  Google Scholar 

  33. Barber AC et al (2013) Repair of the degenerate retina by photoreceptor transplantation. Proc Natl Acad Sci U S A 110(1):354–359

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  34. Pearson RA et al (2012) Restoration of vision after transplantation of photoreceptors. Nature 485(7396):99–103

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  35. MacLaren RE et al (2006) Retinal repair by transplantation of photoreceptor precursors. Nature 444(7116):203–207

    Article  CAS  PubMed  Google Scholar 

  36. Bainbridge JW et al (2008) Effect of gene therapy on visual function in Leber’s congenital amaurosis. N Engl J Med 358(21):2231–2239

    Article  CAS  PubMed  Google Scholar 

  37. Locker M, El Yakoubi W, Mazurier N, Dullin JP, Perron M (2010) A decade of mammalian retinal stem cell research. Arch Ital Biol 148(2):59–72

    CAS  PubMed  Google Scholar 

  38. Ramsden CM et al (2013) Stem cells in retinal regeneration: past, present and future. Development 140(12):2576–2585

    Article  CAS  PubMed  Google Scholar 

  39. Karl MO (2013) The potential of stem cell research for the treatment of neuronal damage in glaucoma. Cell Tissue Res 353(2):311–325

    Article  PubMed  Google Scholar 

  40. Lamba D, Karl M, Reh T (2008) Neural regeneration and cell replacement: a view from the eye. Cell Stem Cell 2(6):538–549

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  41. Easter SS Jr (2000) Let there be sight. Neuron 27(2):193–195

    Article  CAS  PubMed  Google Scholar 

  42. Schmidt R, Strahle U, Scholpp S (2013) Neurogenesis in zebrafish—from embryo to adult. Neural Dev 8:3

    Article  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  44. Hitchcock PF, Raymond PA (2004) The teleost retina as a model for developmental and regeneration biology. Zebrafish 1(3):257–271

    Article  PubMed  Google Scholar 

  45. Kuhrt H et al (2012) Postnatal mammalian retinal development: quantitative data and general rules. Prog Retin Eye Res 31(6):605–621

    Article  PubMed  Google Scholar 

  46. Wetts R, Fraser SE (1988) Multipotent precursors can give rise to all major cell types of the frog retina. Science 239(4844):1142–1145

    Article  CAS  PubMed  Google Scholar 

  47. Wetts R, Serbedzija GN, Fraser SE (1989) Cell lineage analysis reveals multipotent precursors in the ciliary margin of the frog retina. Dev Biol 136(1):254–263

    Article  CAS  PubMed  Google Scholar 

  48. 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 Central  PubMed  CAS  Google Scholar 

  49. Johns PR (1977) Growth of the adult goldfish eye. III. Source of the new retinal cells. J Comp Neurol 176(3):343–357

    Article  CAS  PubMed  Google Scholar 

  50. 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(1–2):31–41

    Article  CAS  PubMed  Google Scholar 

  51. Straznicky K, Gaze RM (1971) The growth of the retina in Xenopus laevis: an autoradiographic study. J Embryol Exp Morphol 26(1):67–79

    CAS  PubMed  Google Scholar 

  52. Raymond PA, Easter SS Jr (1983) Postembryonic growth of the optic tectum in goldfish. I. Location of germinal cells and numbers of neurons produced. J Neurosci 3(5):1077–1091

    CAS  PubMed  Google Scholar 

  53. Bringmann A et al (2006) Muller cells in the healthy and diseased retina. Prog Retin Eye Res 25(4):397–424

    Article  CAS  PubMed  Google Scholar 

  54. Jadhav AP, Roesch K, Cepko CL (2009) Development and neurogenic potential of Muller glial cells in the vertebrate retina. Prog Retin Eye Res 28(4):249–262

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  55. Newman E, Reichenbach A (1996) The Muller cell: a functional element of the retina. Trends Neurosci 19(8):307–312

    Article  CAS  PubMed  Google Scholar 

  56. Bringmann A, Schopf S, Reichenbach A (2000) Developmental regulation of calcium channel-mediated currents in retinal glial (Muller) cells. J Neurophysiol 84(6):2975–2983

    CAS  PubMed  Google Scholar 

  57. Mata NL, Radu RA, Clemmons RC, Travis GH (2002) Isomerization and oxidation of vitamin a in cone-dominant retinas: a novel pathway for visual-pigment regeneration in daylight. Neuron 36(1):69–80

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  58. Johns PR, Fernald RD (1981) Genesis of rods in teleost fish retina. Nature 293(5828):141–142

    Article  CAS  PubMed  Google Scholar 

  59. Julian D, Ennis K, Korenbrot JI (1998) Birth and fate of proliferative cells in the inner nuclear layer of the mature fish retina. J Comp Neurol 394(3):271–282

    Article  CAS  PubMed  Google Scholar 

  60. 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(26):7028–7040

    Article  CAS  PubMed  Google Scholar 

  61. Raymond PA, Rivlin PK (1987) Germinal cells in the goldfish retina that produce rod photoreceptors. Dev Biol 122(1):120–138

    Article  CAS  PubMed  Google Scholar 

  62. 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(1):62–76

    Article  CAS  PubMed  Google Scholar 

  63. Maier W, Wolburg H (1979) Regeneration of the goldfish retina after exposure to different doses of ouabain. Cell Tissue Res 202(1):99–118

    Article  CAS  PubMed  Google Scholar 

  64. Hitchcock PF, Raymond PA (1992) Retinal regeneration. Trends Neurosci 15(3):103–108

    Article  CAS  PubMed  Google Scholar 

  65. Braisted JE, Essman TF, Raymond PA (1994) Selective regeneration of photoreceptors in goldfish retina. Development 120(9):2409–2419

    CAS  PubMed  Google Scholar 

  66. Fausett BV, Goldman D (2006) A role for alpha1 tubulin-expressing Muller glia in regeneration of the injured zebrafish retina. J Neurosci 26(23):6303–6313

    Article  CAS  PubMed  Google Scholar 

  67. Wu DM et al (2001) Cones regenerate from retinal stem cells sequestered in the inner nuclear layer of adult goldfish retina. Invest Ophthalmol Vis Sci 42(9):2115–2124

    CAS  PubMed  Google Scholar 

  68. Yurco P, Cameron DA (2005) Responses of Muller glia to retinal injury in adult zebrafish. Vision Res 45(8):991–1002

    Article  PubMed  Google Scholar 

  69. Thummel R et al (2008) Characterization of Muller glia and neuronal progenitors during adult zebrafish retinal regeneration. Exp Eye Res 87(5):433–444

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  70. Fischer AJ, Reh TA (2003) Potential of Muller glia to become neurogenic retinal progenitor cells. Glia 43(1):70–76

    Article  PubMed  Google Scholar 

  71. Fischer AJ, Reh TA (2001) Muller glia are a potential source of neural regeneration in the postnatal chicken retina. Nat Neurosci 4(3):247–252

    Article  CAS  PubMed  Google Scholar 

  72. Hayes S, Nelson BR, Buckingham B, Reh TA (2007) Notch signaling regulates regeneration in the avian retina. Dev Biol 312(1):300–311

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  73. Bringmann A et al (2009) Cellular signaling and factors involved in Muller cell gliosis: neuroprotective and detrimental effects. Prog Retin Eye Res 28(6):423–451

    Article  CAS  PubMed  Google Scholar 

  74. Wan J et al (2008) Preferential regeneration of photoreceptor from Muller glia after retinal degeneration in adult rat. Vision Res 48(2):223–234

    Article  CAS  PubMed  Google Scholar 

  75. Tropepe V et al (2000) Retinal stem cells in the adult mammalian eye. Science 287(5460):2032–2036

    Article  CAS  PubMed  Google Scholar 

  76. Das AV et al (2006) Neural stem cell properties of Muller glia in the mammalian retina: regulation by Notch and Wnt signaling. Dev Biol 299(1):283–302

    Article  CAS  PubMed  Google Scholar 

  77. Bhatia B, Jayaram H, Singhal S, Jones MF, Limb GA (2011) Differences between the neurogenic and proliferative abilities of Muller glia with stem cell characteristics and the ciliary epithelium from the adult human eye. Exp Eye Res 93(6):852–861

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  78. Lawrence JM et al (2007) MIO-M1 cells and similar muller glial cell lines derived from adult human retina exhibit neural stem cell characteristics. Stem Cells 25(8):2033–2043

    Article  CAS  PubMed  Google Scholar 

  79. Cameron DA, Easter SS Jr (1995) Cone photoreceptor regeneration in adult fish retina: phenotypic determination and mosaic pattern formation. J Neurosci 15(3 pt 2):2255–2271

    CAS  PubMed  Google Scholar 

  80. Faillace MP, Julian D, Korenbrot JI (2002) Mitotic activation of proliferative cells in the inner nuclear layer of the mature fish retina: regulatory signals and molecular markers. J Comp Neurol 451(2):127–141

    Article  CAS  PubMed  Google Scholar 

  81. Senut MC, Gulati-Leekha A, Goldman D (2004) 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. J Neurosci 24(35):7663–7673

    Article  CAS  PubMed  Google Scholar 

  82. Hieber V, Agranoff BW, Goldman D (1992) Target-dependent regulation of retinal nicotinic acetylcholine receptor and tubulin RNAs during optic nerve regeneration in goldfish. J Neurochem 58(3):1009–1015

    Article  CAS  PubMed  Google Scholar 

  83. Penn JS (1985) Effects of continuous light on the retina of a fish, Notemigonus crysoleucas. J Comp Neurol 238(1):121–127

    Article  CAS  PubMed  Google Scholar 

  84. Abler AS, Chang CJ, Ful J, Tso MO, Lam TT (1996) Photic injury triggers apoptosis of photoreceptor cells. Res Commun Mol Pathol Pharmacol 92(2):177–189

    CAS  PubMed  Google Scholar 

  85. 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(3):289–307

    Article  CAS  PubMed  Google Scholar 

  86. Fimbel SM, Montgomery JE, Burket CT, Hyde DR (2007) Regeneration of inner retinal neurons after intravitreal injection of ouabain in zebrafish. J Neurosci 27(7):1712–1724

    Article  CAS  PubMed  Google Scholar 

  87. Sherpa T et al (2008) Ganglion cell regeneration following whole-retina destruction in zebrafish. Dev Neurobiol 68(2):166–181

    Article  PubMed Central  PubMed  Google Scholar 

  88. Dvorak DR, Morgan IG (1983) Intravitreal kainic acid permanently eliminates off-pathways from chicken retina. Neurosci Lett 36(3):249–253

    Article  CAS  PubMed  Google Scholar 

  89. Ingham CA, Morgan IG (1983) Dose-dependent effects of intravitreal kainic acid on specific cell types in chicken retina. Neuroscience 9(1):165–181

    Article  CAS  PubMed  Google Scholar 

  90. Morgan IG (1981) Intraocular colchicine selectively destroys immature ganglion cells in chicken retina. Neurosci Lett 24(3):255–260

    Article  CAS  PubMed  Google Scholar 

  91. Fischer AJ, Reh TA (2002) Exogenous growth factors stimulate the regeneration of ganglion cells in the chicken retina. Dev Biol 251(2):367–379

    Article  CAS  PubMed  Google Scholar 

  92. Fischer AJ, Seltner RL, Poon J, Stell WK (1998) Immunocytochemical characterization of quisqualic acid- and N-methyl-D-aspartate-induced excitotoxicity in the retina of chicks. J Comp Neurol 393(1):1–15

    Article  CAS  PubMed  Google Scholar 

  93. Tappeiner C et al (2013) Characteristics of rod regeneration in a novel zebrafish retinal degeneration model using N-methyl-N-nitrosourea (MNU). PLoS One 8(8):e71064

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  94. Curado S, Stainier DY, Anderson RM (2008) Nitroreductase-mediated cell/tissue ablation in zebrafish: a spatially and temporally controlled ablation method with applications in developmental and regeneration studies. Nat Protoc 3(6):948–954

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  95. Scott EK, Baier H (2009) The cellular architecture of the larval zebrafish tectum, as revealed by gal4 enhancer trap lines. Front Neural Circuits 3:13

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  96. Zhao XF, Ellingsen S, Fjose A (2009) Labelling and targeted ablation of specific bipolar cell types in the zebrafish retina. BMC Neurosci 10:107

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  97. 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(6):800–814

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  98. 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)

    Google Scholar 

  99. Fleisch VC, Fraser B, Allison WT (2011) Investigating regeneration and functional integration of CNS neurons: lessons from zebrafish genetics and other fish species. Biochim Biophys Acta 1812(3):364–380

    Article  CAS  PubMed  Google Scholar 

  100. Nelson CM, Hyde DR (2012) Muller glia as a source of neuronal progenitor cells to regenerate the damaged zebrafish retina. Adv Exp Med Biol 723:425–430

    Article  CAS  PubMed  Google Scholar 

  101. Vihtelic TS, Soverly JE, Kassen SC, Hyde DR (2006) Retinal regional differences in photoreceptor cell death and regeneration in light-lesioned albino zebrafish. Exp Eye Res 82(4):558–575

    Article  CAS  PubMed  Google Scholar 

  102. 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(5):605–619

    Article  PubMed Central  PubMed  Google Scholar 

  103. Kassen SC et al (2007) Time course analysis of gene expression during light-induced photoreceptor cell death and regeneration in albino zebrafish. Dev Neurobiol 67(8):1009–1031

    Article  CAS  PubMed  Google Scholar 

  104. Miller B, Miller H, Ryan SJ (1986) Experimental epiretinal proliferation induced by intravitreal red blood cells. Am J Ophthalmol 102(2):188–195

    Article  CAS  PubMed  Google Scholar 

  105. Algvere P, Kock E (1983) Experimental epiretinal membranes induced by intravitreal carbon particles. Am J Ophthalmol 96(3):345–353

    CAS  PubMed  Google Scholar 

  106. Friedenwald JS, Chan E (1932) Pathogenesis of retinitis pigmentosa with a note on the phagocytic activity of Muller’s fibers. Arch Ophthalmol 8:173–181

    Article  Google Scholar 

  107. Rosenthal AR, Appleton B (1975) Histochemical localization of intraocular copper foreign bodies. Am J Ophthalmol 79(4):613–625

    CAS  PubMed  Google Scholar 

  108. Wagner EC, Raymond PA (1991) Muller glial cells of the goldfish retina are phagocytic in vitro but not in vivo. Exp Eye Res 53(5):583–589

    Article  CAS  PubMed  Google Scholar 

  109. Mano T, Puro DG (1990) Phagocytosis by human retinal glial cells in culture. Invest Ophthalmol Vis Sci 31(6):1047–1055

    CAS  PubMed  Google Scholar 

  110. Francke M et al (2001) Retinal pigment epithelium melanin granules are phagocytozed by Muller glial cells in experimental retinal detachment. J Neurocytol 30(2):131–136

    Article  CAS  PubMed  Google Scholar 

  111. Morris AC, Schroeter EH, Bilotta J, Wong RO, Fadool JM (2005) Cone survival despite rod degeneration in XOPS-mCFP transgenic zebrafish. Invest Ophthalmol Vis Sci 46(12):4762–4771

    Article  PubMed Central  PubMed  Google Scholar 

  112. Egensperger R, Maslim J, Bisti S, Hollander H, Stone J (1996) Fate of DNA from retinal cells dying during development: uptake by microglia and macroglia (Muller cells). Brain Res Dev Brain Res 97(1):1–8

    Article  CAS  PubMed  Google Scholar 

  113. 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(5):601–612

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  114. Meyers JR et al (2012) Beta-catenin/Wnt signaling controls progenitor fate in the developing and regenerating zebrafish retina. Neural Dev 7:30

    Article  PubMed Central  PubMed  Google Scholar 

  115. Gorsuch RA, Hyde DR (2013) Regulation of Müller glia dependent neuronal regeneration in the damaged adult zebrafish retina. Exp Eye Res (in press)

    Google Scholar 

  116. 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(6):1858–1866

    Article  CAS  PubMed  Google Scholar 

  117. Ghai K, Zelinka C, Fischer AJ (2010) Notch signaling influences neuroprotective and proliferative properties of mature Muller glia. J Neurosci 30(8):3101–3112

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  118. Nelson CM et al (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(18):4294–4311

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  119. Roesch K et al (2008) The transcriptome of retinal Muller glial cells. J Comp Neurol 509(2):225–238

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  120. Mizutani M, Gerhardinger C, Lorenzi M (1998) Muller cell changes in human diabetic retinopathy. Diabetes 47(3):445–449

    Article  CAS  PubMed  Google Scholar 

  121. Chen H, Weber AJ (2002) Expression of glial fibrillary acidic protein and glutamine synthetase by Müller cells after optic nerve damage and intravitreal application of brain-derived neurotrophic factor. GLIA 38(2):115–125

    Article  PubMed  Google Scholar 

  122. Qin Z, Barthel LK, Raymond PA (2009) Genetic evidence for shared mechanisms of epimorphic regeneration in zebrafish. Proc Natl Acad Sci U S A 106(23):9310–9315

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  123. Kacza J et al (2000) Neuron-glia interactions in the rat retina infected by Borna disease virus. Arch Virol 145(1):127–147

    Article  CAS  PubMed  Google Scholar 

  124. Hartig W et al (1995) Alterations of Muller (glial) cells in dystrophic retinae of RCS rats. J Neurocytol 24(7):507–517

    Article  CAS  PubMed  Google Scholar 

  125. Geller SF, Lewis GP, Anderson DH, Fisher SK (1995) Use of the MIB-1 antibody for detecting proliferating cells in the retina. Invest Ophthalmol Vis Sci 36(3):737–744

    CAS  PubMed  Google Scholar 

  126. Fisher SK, Erickson PA, Lewis GP, Anderson DH (1991) Intraretinal proliferation induced by retinal detachment. Invest Ophthalmol Vis Sci 32(6):1739–1748

    CAS  PubMed  Google Scholar 

  127. Lieth E et al (1998) Glial reactivity and impaired glutamate metabolism in short-term experimental diabetic retinopathy. Penn State Retina Research Group. Diabetes 47(5):815–820

    Article  CAS  PubMed  Google Scholar 

  128. Joly S, Lange C, Thiersch M, Samardzija M, Grimm C (2008) Leukemia inhibitory factor extends the lifespan of injured photoreceptors in vivo. J Neurosci 28(51):13765–13774

    Article  CAS  PubMed  Google Scholar 

  129. Garcia M, Vecino E (2003) Role of Muller glia in neuroprotection and regeneration in the retina. Histol Histopathol 18(4):1205–1218

    CAS  PubMed  Google Scholar 

  130. Verardo MR et al (2008) Abnormal reactivity of muller cells after retinal detachment in mice deficient in GFAP and vimentin. Invest Ophthalmol Vis Sci 49(8):3659–3665

    Article  PubMed Central  PubMed  Google Scholar 

  131. Kyritsis N et al (2012) Acute inflammation initiates the regenerative response in the adult zebrafish brain. Science 338(6112):1353–1356

    Article  CAS  PubMed  Google Scholar 

  132. Thomas JL, Nelson CM, Luo X, Hyde DR, Thummel R (2012) Characterization of multiple light damage paradigms reveals regional differences in photoreceptor loss. Exp Eye Res 97(1):105–116

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  133. Cameron DA, Carney LH (2000) Cell mosaic patterns in the native and regenerated inner retina of zebrafish: implications for retinal assembly. J Comp Neurol 416(3):356–367

    Article  CAS  PubMed  Google Scholar 

  134. Kassen SC et al (2008) The Tg(ccnb1:EGFP) transgenic zebrafish line labels proliferating cells during retinal development and regeneration. Mol Vis 14:951–963

    PubMed Central  PubMed  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(2):334–347

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  136. Cameron DA, Gentile KL, Middleton FA, Yurco P (2005) Gene expression profiles of intact and regenerating zebrafish retina. Mol Vis 11:775–791

    CAS  PubMed  Google Scholar 

  137. Lenkowski JR et al (2013) Retinal regeneration in adult zebrafish requires regulation of TGFbeta signaling. Glia 61(10):1687–1697

    Article  PubMed  Google Scholar 

  138. Nelson CM et al (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(15):6524–6539

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  139. Fausett BV, Gumerson JD, Goldman D (2008) The proneural basic helix-loop-helix gene ascl1a is required for retina regeneration. J Neurosci 28(5):1109–1117

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  140. 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(11):1101–1107

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  141. Pollak J et al (2013) ASCL1 reprograms mouse Muller glia into neurogenic retinal progenitors. Development 140(12):2619–2631

    Article  CAS  PubMed  Google Scholar 

  142. Livesey FJ, Young TL, Cepko CL (2004) An analysis of the gene expression program of mammalian neural progenitor cells. Proc Natl Acad Sci U S A 101(5):1374–1379

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  143. Levine EM, Hitchcock PF, Glasgow E, Schechter N (1994) Restricted expression of a new paired-class homeobox gene in normal and regenerating adult goldfish retina. J Comp Neurol 348(4):596–606

    Article  CAS  PubMed  Google Scholar 

  144. Hitchcock PF, Macdonald RE, VanDeRyt JT, Wilson SW (1996) Antibodies against Pax6 immunostain amacrine and ganglion cells and neuronal progenitors, but not rod precursors, in the normal and regenerating retina of the goldfish. J Neurobiol 29(3):399–413

    Article  CAS  PubMed  Google Scholar 

  145. 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(3):208–223

    Article  CAS  PubMed  Google Scholar 

  146. Liu Q et al (2002) Up-regulation of cadherin-2 and cadherin-4 in regenerating visual structures of adult zebrafish. Exp Neurol 177(2):396–406

    Article  CAS  PubMed  Google Scholar 

  147. Marquardt T et al (2001) Pax6 is required for the multipotent state of retinal progenitor cells. Cell 105(1):43–55

    Article  CAS  PubMed  Google Scholar 

  148. Wan J, Zheng H, Xiao HL, She ZJ, Zhou GM (2007) Sonic hedgehog promotes stem-cell potential of Muller glia in the mammalian retina. Biochem Biophys Res Commun 363(2):347–354

    Article  CAS  PubMed  Google Scholar 

  149. Ooto S et al (2004) Potential for neural regeneration after neurotoxic injury in the adult mammalian retina. Proc Natl Acad Sci U S A 101(37):13654–13659

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  150. Close JL, Liu J, Gumuscu B, Reh TA (2006) Epidermal growth factor receptor expression regulates proliferation in the postnatal rat retina. Glia 54(2):94–104

    Article  PubMed  Google Scholar 

  151. Osakada F et al (2007) Wnt signaling promotes regeneration in the retina of adult mammals. J Neurosci 27(15):4210–4219

    Article  CAS  PubMed  Google Scholar 

  152. Karl MO et al (2008) Stimulation of neural regeneration in the mouse retina. Proc Natl Acad Sci U S A 105(49):19508–19513

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  153. Bhatia B, Singhal S, Lawrence JM, Khaw PT, Limb GA (2009) Distribution of Muller stem cells within the neural retina: evidence for the existence of a ciliary margin-like zone in the adult human eye. Exp Eye Res 89(3):373–382

    Article  CAS  PubMed  Google Scholar 

  154. Blackshaw S et al (2004) Genomic analysis of mouse retinal development. PLoS Biol 2(9):E247

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  155. Trimarchi JM, Stadler MB, Cepko CL (2008) Individual retinal progenitor cells display extensive heterogeneity of gene expression. PLoS One 3(2):e1588

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  156. 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(3):1096–1109

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  157. Thummel R et al (2010) Pax6a and Pax6b are required at different points in neuronal progenitor cell proliferation during zebrafish photoreceptor regeneration. Exp Eye Res 90(5):572–582

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  158. Xu S et al (2007) The proliferation and expansion of retinal stem cells require functional Pax6. Dev Biol 304(2):713–721

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  159. 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(10):1013–1023

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  160. Wehman AM, Staub W, Meyers JR, Raymond PA, Baier H (2005) Genetic dissection of the zebrafish retinal stem-cell compartment. Dev Biol 281(1):53–65

    Article  CAS  PubMed  Google Scholar 

  161. He J et al (2012) How variable clones build an invariant retina. Neuron 75(5):786–798

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  162. Young RW (1985) Cell proliferation during postnatal development of the retina in the mouse. Brain Res 353(2):229–239

    Article  CAS  PubMed  Google Scholar 

  163. Baye LM, Link BA (2007) Interkinetic nuclear migration and the selection of neurogenic cell divisions during vertebrate retinogenesis. J Neurosci 27(38):10143–10152

    Article  CAS  PubMed  Google Scholar 

  164. Del Bene F, Wehman AM, Link BA, Baier H (2008) Regulation of neurogenesis by interkinetic nuclear migration through an apical-basal notch gradient. Cell 134(6):1055–1065

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  165. Norden C, Young S, Link BA, Harris WA (2009) Actomyosin is the main driver of interkinetic nuclear migration in the retina. Cell 138(6):1195–1208

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  166. Randlett O, Norden C, Harris WA (2010) The vertebrate retina: a model for neuronal polarization in vivo. Dev Neurobiol 71(6):567–583

    Article  Google Scholar 

  167. 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. Proc Natl Acad Sci U S A 108(38):15858–15863

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  168. Inoue T et al (2006) Activation of canonical Wnt pathway promotes proliferation of retinal stem cells derived from adult mouse ciliary margin. Stem Cells 24(1):95–104

    Article  CAS  PubMed  Google Scholar 

  169. Kubo F, Nakagawa S (2009) Hairy1 acts as a node downstream of Wnt signaling to maintain retinal stem cell-like progenitor cells in the chick ciliary marginal zone. Development 136(11):1823–1833

    Article  CAS  PubMed  Google Scholar 

  170. Moshiri A, Close J, Reh TA (2004) Retinal stem cells and regeneration. Int J Dev Biol 48(8–9):1003–1014

    Article  PubMed  Google Scholar 

  171. Shkumatava A, Neumann CJ (2005) Shh directs cell-cycle exit by activating p57Kip2 in the zebrafish retina. EMBO Rep 6(6):563–569

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  172. Locker M et al (2006) Hedgehog signaling and the retina: insights into the mechanisms controlling the proliferative properties of neural precursors. Genes Dev 20(21):3036–3048

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  173. Jian Q et al (2009) Activation of retinal stem cells in the proliferating marginal region of RCS rats during development of retinitis pigmentosa. Neurosci Lett 465(1):41–44

    Article  CAS  PubMed  Google Scholar 

  174. Pearson R, Catsicas M, Becker D, Mobbs P (2002) Purinergic and muscarinic modulation of the cell cycle and calcium signaling in the chick retinal ventricular zone. J Neurosci 22(17):7569–7579

    CAS  PubMed  Google Scholar 

  175. Pearson RA, Dale N, Llaudet E, Mobbs P (2005) ATP released via gap junction hemichannels from the pigment epithelium regulates neural retinal progenitor proliferation. Neuron 46(5):731–744

    Article  CAS  PubMed  Google Scholar 

  176. Nunes PH et al (2007) Signal transduction pathways associated with ATP-induced proliferation of cell progenitors in the intact embryonic retina. Int J Dev Neurosci 25(8):499–508

    Article  CAS  PubMed  Google Scholar 

  177. 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(2):600–613

    Article  CAS  PubMed  Google Scholar 

  178. Kassen SC et al (2009) CNTF induces photoreceptor neuroprotection and Muller glial cell proliferation through two different signaling pathways in the adult zebrafish retina. Exp Eye Res 88(6):1051–1064

    Article  CAS  PubMed  Google Scholar 

  179. Calinescu AA, Vihtelic TS, Hyde DR, Hitchcock PF (2009) Cellular expression of midkine-a and midkine-b during retinal development and photoreceptor regeneration in zebrafish. J Comp Neurol 514(1):1–10

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  180. Luo J et al (2012) Midkine-A functions upstream of Id2a to regulate cell cycle kinetics in the developing vertebrate retina. Neural Dev 7(1):33

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  181. Uribe RA, Gross JM (2010) Id2a influences neuron and glia formation in the zebrafish retina by modulating retinoblast cell cycle kinetics. Development 137(22):3763–3774

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  182. Uribe RA, Kwon T, Marcotte EM, Gross JM (2012) Id2a functions to limit Notch pathway activity and thereby influence the transition from proliferation to differentiation of retinoblasts during zebrafish retinogenesis. Dev Biol 371(2):280–292

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  183. Yurco P, Cameron DA (2007) Cellular correlates of proneural and Notch-delta gene expression in the regenerating zebrafish retina. Vis Neurosci 24(3):437–443

    Article  PubMed  Google Scholar 

  184. Song WT, Zhang XY, Xia XB (2013) Atoh7 promotes the differentiation of retinal stem cells derived from Muller cells into retinal ganglion cells by inhibiting Notch signaling. Stem Cell Res Ther 4(4):94

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  185. Inoue T et al (2002) Math3 and NeuroD regulate amacrine cell fate specification in the retina. Development 129(4):831–842

    CAS  PubMed  Google Scholar 

  186. 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(1):e55410

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  187. Otteson DC, Hitchcock PF (2003) Stem cells in the teleost retina: persistent neurogenesis and injury-induced regeneration. Vision Res 43(8):927–936

    Article  CAS  PubMed  Google Scholar 

  188. DeCarvalho AC, Cappendijk SL, Fadool JM (2004) Developmental expression of the POU domain transcription factor Brn-3b (Pou4f2) in the lateral line and visual system of zebrafish. Dev Dyn 229(4):869–876

    Article  PubMed  CAS  Google Scholar 

  189. Stenkamp DL, Frey RA (2003) Extraretinal and retinal hedgehog signaling sequentially regulate retinal differentiation in zebrafish. Dev Biol 258(2):349–363

    Article  CAS  PubMed  Google Scholar 

  190. Neumann CJ, Nuesslein-Volhard C (2000) Patterning of the zebrafish retina by a wave of sonic hedgehog activity. Science 289(5487):2137–2139

    Article  CAS  PubMed  Google Scholar 

  191. Craig SE et al (2010) The zebrafish galectin Drgal1-l2 is expressed by proliferating Muller glia and photoreceptor progenitors and regulates the regeneration of rod photoreceptors. Invest Ophthalmol Vis Sci 51(6):3244–3252

    Article  PubMed Central  PubMed  Google Scholar 

  192. Bailey TJ, Davis DH, Vance JE, Hyde DR (2012) Spectral-domain optical coherence tomography as a noninvasive method to assess damaged and regenerating adult zebrafish retinas. Invest Ophthalmol Vis Sci 53(6):3126–3138

    Article  PubMed Central  PubMed  Google Scholar 

  193. Wanner M et al (1995) Reevaluation of the growth-permissive substrate properties of goldfish optic nerve myelin and myelin proteins. J Neurosci 15(11):7500–7508

    CAS  PubMed  Google Scholar 

  194. Becker CG, Becker T (2002) Repellent guidance of regenerating optic axons by chondroitin sulfate glycosaminoglycans in zebrafish. J Neurosci 22(3):842–853

    CAS  PubMed  Google Scholar 

  195. Vidal-Sanz M, Bray GM, Villegas-Perez MP, Thanos S, Aguayo AJ (1987) Axonal regeneration and synapse formation in the superior colliculus by retinal ganglion cells in the adult rat. J Neurosci 7(9):2894–2909

    CAS  PubMed  Google Scholar 

  196. Villegas-Perez MP, Vidal-Sanz M, Bray GM, Aguayo AJ (1988) Influences of peripheral nerve grafts on the survival and regrowth of axotomized retinal ganglion cells in adult rats. J Neurosci 8(1):265–280

    CAS  PubMed  Google Scholar 

  197. Fawcett JW (2006) Overcoming inhibition in the damaged spinal cord. J Neurotrauma 23(3–4):371–383

    Article  PubMed  Google Scholar 

  198. Silver J, Miller JH (2004) Regeneration beyond the glial scar. Nat Rev Neurosci 5(2):146–156

    Article  CAS  PubMed  Google Scholar 

  199. Springer AD (1981) Normal and abnormal retinal projections following the crush of one optic nerve in goldfish (Carassius auratus). J Comp Neurol 199(1):87–95

    Article  CAS  PubMed  Google Scholar 

  200. Becker CG, Meyer RL, Becker T (2000) Gradients of ephrin-A2 and ephrin-A5b mRNA during retinotopic regeneration of the optic projection in adult zebrafish. J Comp Neurol 427(3):469–483

    Article  CAS  PubMed  Google Scholar 

  201. Schmidt JT (2004) Activity-driven sharpening of the retinotectal projection: the search for retrograde synaptic signaling pathways. J Neurobiol 59(1):114–133

    Article  CAS  PubMed  Google Scholar 

  202. Saszik S, Bilotta J, Givin CM (1999) ERG assessment of zebrafish retinal development. Vis Neurosci 16(5):881–888

    Article  CAS  PubMed  Google Scholar 

  203. Makhankov YV, Rinner O, Neuhauss SC (2004) An inexpensive device for non-invasive electroretinography in small aquatic vertebrates. J Neurosci Methods 135(1–2):205–210

    Article  PubMed  Google Scholar 

  204. Mensinger AF, Powers MK (2007) Visual function in regenerating teleost retina following surgical lesioning. Vis Neurosci 24(3):299–307

    Article  PubMed  Google Scholar 

  205. Allison WT, Dann SG, Veldhoen KM, Hawryshyn CW (2006) Degeneration and regeneration of ultraviolet cone photoreceptors during development in rainbow trout. J Comp Neurol 499(5):702–715

    Article  CAS  PubMed  Google Scholar 

  206. Kastner R, Wolburg H (1982) Functional regeneration of the visual system in teleosts. Comparative investigations after optic nerve crush and damage of the retina. Z Naturforsch C 37(11–12):1274–1280

    CAS  PubMed  Google Scholar 

  207. Mensinger AF, Powers MK (1999) Visual function in regenerating teleost retina following cytotoxic lesioning. Vis Neurosci 16(2):241–251

    Article  CAS  PubMed  Google Scholar 

  208. Li L, Dowling JE (1997) A dominant form of inherited retinal degeneration caused by a non-photoreceptor cell-specific mutation. Proc Natl Acad Sci U S A 94(21):11645–11650

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  209. Rinner O, Rick JM, Neuhauss SC (2005) Contrast sensitivity, spatial and temporal tuning of the larval zebrafish optokinetic response. Invest Ophthalmol Vis Sci 46(1):137–142

    Article  PubMed  Google Scholar 

  210. Brockerhoff SE (2006) Measuring the optokinetic response of zebrafish larvae. Nat Protoc 1(5):2448–2451

    Article  CAS  PubMed  Google Scholar 

  211. Takeda M et al (2008) alpha-Aminoadipate induces progenitor cell properties of Muller glia in adult mice. Invest Ophthalmol Vis Sci 49(3):1142–1150

    Article  PubMed Central  PubMed  Google Scholar 

  212. Chacko DM et al (2003) Transplantation of ocular stem cells: the role of injury in incorporation and differentiation of grafted cells in the retina. Vision Res 43(8):937–946

    Article  PubMed  Google Scholar 

  213. Kostyk SK, D’Amore PA, Herman IM, Wagner JA (1994) Optic nerve injury alters basic fibroblast growth factor localization in the retina and optic tract. J Neurosci 14(3 pt 2):1441–1449

    CAS  PubMed  Google Scholar 

  214. Wen R et al (1995) Injury-induced upregulation of bFGF and CNTF mRNAS in the rat retina. J Neurosci 15(11):7377–7385

    CAS  PubMed  Google Scholar 

  215. Valter K, Maslim J, Bowers F, Stone J (1998) Photoreceptor dystrophy in the RCS rat: roles of oxygen, debris, and bFGF. Invest Ophthalmol Vis Sci 39(12):2427–2442

    CAS  PubMed  Google Scholar 

  216. Walsh N, Valter K, Stone J (2001) Cellular and subcellular patterns of expression of bFGF and CNTF in the normal and light stressed adult rat retina. Exp Eye Res 72(5):495–501

    Article  CAS  PubMed  Google Scholar 

  217. Cao W, Li F, Steinberg RH, Lavail MM (2001) Development of normal and injury-induced gene expression of aFGF, bFGF, CNTF, BDNF, GFAP and IGF-I in the rat retina. Exp Eye Res 72(5):591–604

    Article  CAS  PubMed  Google Scholar 

  218. Hochmann S et al (2012) Fgf signaling is required for photoreceptor maintenance in the adult zebrafish retina. PLoS One 7(1):e30365

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  219. Qin Z et al (2011) FGF signaling regulates rod photoreceptor cell maintenance and regeneration in zebrafish. Exp Eye Res 93(5):726–734

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  220. Yang EV, Wang L, Tassava RA (2005) Effects of exogenous FGF-1 treatment on regeneration of the lens and the neural retina in the newt, Notophthalmus viridescens. J Exp Zool A Comp Exp Biol 303(10):837–844

    Article  PubMed  CAS  Google Scholar 

  221. Spence JR, Aycinena JC, Del Rio-Tsonis K (2007) Fibroblast growth factor-hedgehog interdependence during retina regeneration. Dev Dyn 236(5):1161–1174

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  222. Spence JR et al (2004) The hedgehog pathway is a modulator of retina regeneration. Development 131(18):4607–4621

    Article  CAS  PubMed  Google Scholar 

  223. Hansson HA, Holmgren A, Norstedt G, Rozell B (1989) Changes in the distribution of insulin-like growth factor I, thioredoxin, thioredoxin reductase and ribonucleotide reductase during the development of the retina. Exp Eye Res 48(3):411–420

    Article  CAS  PubMed  Google Scholar 

  224. de la Rosa EJ et al (1994) Insulin and insulin-like growth factor system components gene expression in the chicken retina from early neurogenesis until late development and their effect on neuroepithelial cells. Eur J Neurosci 6(12):1801–1810

    Article  PubMed  Google Scholar 

  225. Del Debbio CB et al (2010) Notch and Wnt signaling mediated rod photoreceptor regeneration by Muller cells in adult mammalian retina. PLoS One 5(8):e12425

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  226. 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 U S A 104(51):20380–20385

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  227. Ueki Y, Reh TA (2013) EGF stimulates Muller glial proliferation via a BMP-dependent mechanism. Glia 61(5):778–789

    Article  PubMed Central  PubMed  Google Scholar 

  228. Lima L, Drujan B, Matus P (1990) Spatial distribution of taurine in the teleost retina and its role in retinal tissue regeneration. Prog Clin Biol Res 351:103–112

    CAS  PubMed  Google Scholar 

  229. Hall CM, Else C, Schechter N (1990) Neuronal intermediate filament expression during neurite outgrowth from explanted goldfish retina: effect of retinoic acid. J Neurochem 55(5):1671–1682

    Article  CAS  PubMed  Google Scholar 

  230. Santos E, Monzon-Mayor M, Romero-Aleman MM, Yanes C (2008) Distribution of neurotrophin-3 during the ontogeny and regeneration of the lizard (Gallotia galloti) visual system. Dev Neurobiol 68(1):31–44

    Article  CAS  PubMed  Google Scholar 

  231. Wen R, Tao W, Li Y, Sieving PA (2012) CNTF and retina. Prog Retin Eye Res 31(2):136–151

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  232. Lorenzetto E et al (2013) Rac1 selective activation improves retina ganglion cell survival and regeneration. PLoS One 8(5):e64350

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  233. Fischer D, He Z, Benowitz LI (2004) Counteracting the Nogo receptor enhances optic nerve regeneration if retinal ganglion cells are in an active growth state. J Neurosci 24(7):1646–1651

    Article  CAS  PubMed  Google Scholar 

  234. Veldman MB, Bemben MA, Goldman D (2010) Tuba1a gene expression is regulated by KLF6/7 and is necessary for CNS development and regeneration in zebrafish. Mol Cell Neurosci 43(4):370–383

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

We are extremely grateful to Alexandra D. Almeida, Ryan MacDonald, Florence D’Orazi and Ashley L. Siegel for comments on this chapter.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Patricia R. Jusuf .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Science+Business Media New York

About this chapter

Cite this chapter

Ng, J., Currie, P.D., Jusuf, P.R. (2014). The Regenerative Potential of the Vertebrate Retina: Lessons from the Zebrafish. In: Pébay, A. (eds) Regenerative Biology of the Eye. Stem Cell Biology and Regenerative Medicine. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-0787-8_3

Download citation

Publish with us

Policies and ethics