1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Genomics and Human Genetics
  4. Volume 20, 2019
  5. Article

Annual Review of Genomics and Human Genetics

Volume 20, 2019

Gene and Induced Pluripotent Stem Cell Therapy for Retinal Diseases

Abstract

Given the importance of visual information to many daily activities, retinal degenerative diseases—which include both inherited conditions (such as retinitis pigmentosa) and acquired conditions (such as age-related macular degeneration)—can have a dramatic impact on human lives. The therapeutic options for these diseases remain limited. Since the discovery of the first causal gene for retinitis pigmentosa almost three decades ago, more than 250 genes have been identified, and gene therapies have been rapidly developed. Simultaneously, stem cell technologies such as induced pluripotent stem cell–based transplantation have advanced and have been applied to the treatment of retinal degenerative diseases. Here, we review recent progress in these expanding fields and discuss the potential for precision medicine in ophthalmic care.

Keyword(s): age-related macular degeneration, cell therapy, gene therapy, iPSC, retinitis pigmentosa
Loading

Article metrics loading...

/content/journals/10.1146/annurev-genom-083118-015043
2019-08-31
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/genom/20/1/annurev-genom-083118-015043.html?itemId=/content/journals/10.1146/annurev-genom-083118-015043&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Ahmad I, Tang L, Pham H 2000. Identification of neural progenitors in the adult mammalian eye. Biochem. Biophys. Res. Commun. 270:517–21
     [Google Scholar]
  2. 2.
    Algvere PV, Gouras P, Dafgard Kopp E 1999. Long-term outcome of RPE allografts in non-immunosuppressed patients with AMD. Eur. J. Ophthalmol. 9:217–30
     [Google Scholar]
  3. 3.
    Allikmets R, Singh N, Sun H, Shroyer NF, Hutchinson A et al. 1997. A photoreceptor cell-specific ATP-binding transporter gene (ABCR) is mutated in recessive Stargardt macular dystrophy. Nat. Genet 15:236–46 Corrigendum 1997. Nat. Genet 17:122
     [Google Scholar]
  4. 4.
    Arai Y, Maeda A, Hirami Y, Ishigami C, Kosugi S et al. 2015. Retinitis pigmentosa with EYS mutations is the most prevalent inherited retinal dystrophy in Japanese populations. J. Ophthalmol. 2015:819760
     [Google Scholar]
  5. 5.
    Assawachananont J, Mandai M, Okamoto S, Yamada C, Eiraku M et al. 2014. Transplantation of embryonic and induced pluripotent stem cell-derived 3D retinal sheets into retinal degenerative mice. Stem Cell Rep 2:662–74
     [Google Scholar]
  6. 6.
    Bainbridge JW, Smith AJ, Barker SS, Robbie S, Henderson R et al. 2008. Effect of gene therapy on visual function in Leber's congenital amaurosis. N. Engl. J. Med. 358:2231–39
     [Google Scholar]
  7. 7.
    Barnea-Cramer AO, Wang W, Lu SJ, Singh MS, Luo C et al. 2016. Function of human pluripotent stem cell-derived photoreceptor progenitors in blind mice. Sci. Rep. 6:29784
     [Google Scholar]
  8. 8.
    Batten ML, Imanishi Y, Tu DC, Doan T, Zhu L et al. 2005. Pharmacological and rAAV gene therapy rescue of visual functions in a blind mouse model of Leber congenital amaurosis. PLOS Med 2:e333
     [Google Scholar]
  9. 9.
    Bi A, Cui J, Ma YP, Olshevskaya E, Pu M et al. 2006. Ectopic expression of a microbial-type rhodopsin restores visual responses in mice with photoreceptor degeneration. Neuron 50:23–33
     [Google Scholar]
  10. 10.
    Boye SL, Peshenko IV, Huang WC, Min SH, McDoom I et al. 2013. AAV-mediated gene therapy in the guanylate cyclase (RetGC1/RetGC2) double knockout mouse model of Leber congenital amaurosis. Hum. Gene Ther. 24:189–202
     [Google Scholar]
  11. 11.
    Burnett JC, Rossi JJ. 2012. RNA-based therapeutics: current progress and future prospects. Chem. Biol. 19:60–71
     [Google Scholar]
  12. 12.
    Byrne LC, Dalkara D, Luna G, Fisher SK, Clerin E et al. 2015. Viral-mediated RdCVF and RdCVFL expression protects cone and rod photoreceptors in retinal degeneration. J. Clin. Investig. 125:105–16
     [Google Scholar]
  13. 13.
    Caporale N, Kolstad KD, Lee T, Tochitsky I, Dalkara D et al. 2011. LiGluR restores visual responses in rodent models of inherited blindness. Mol. Ther. 19:1212–19
     [Google Scholar]
  14. 14.
    Carroll EC, Berlin S, Levitz J, Kienzler MA, Yuan Z et al. 2015. Two-photon brightness of azobenzene photoswitches designed for glutamate receptor optogenetics. PNAS 112:E776–85
     [Google Scholar]
  15. 15.
    Cayouette M, Gravel C. 1997. Adenovirus-mediated gene transfer of ciliary neurotrophic factor can prevent photoreceptor degeneration in the retinal degeneration (rd) mouse. Hum. Gene Ther. 8:423–30
     [Google Scholar]
  16. 16.
    Coles BL, Angenieux B, Inoue T, Del Rio-Tsonis K, Spence JR et al. 2004. Facile isolation and the characterization of human retinal stem cells. PNAS 101:15772–77
     [Google Scholar]
  17. 17.
    da Cruz L, Fynes K, Georgiadis O, Kerby J, Luo YH et al. 2018. Phase 1 clinical study of an embryonic stem cell-derived retinal pigment epithelium patch in age-related macular degeneration. Nat. Biotechnol. 36:328–37
     [Google Scholar]
  18. 18.
    Das T, del Cerro M, Jalali S, Rao VS, Gullapalli VK et al. 1999. The transplantation of human fetal neuroretinal cells in advanced retinitis pigmentosa patients: results of a long-term safety study. Exp. Neurol. 157:58–68
     [Google Scholar]
  19. 19.
    DiCarlo JE, Mahajan VB, Tsang SH 2018. Gene therapy and genome surgery in the retina. J. Clin. Investig. 128:2177–88
     [Google Scholar]
  20. 20.
    Dryja TP, McGee TL, Reichel E, Hahn LB, Cowley GS et al. 1990. A point mutation of the rhodopsin gene in one form of retinitis pigmentosa. Nature 343:364–66
     [Google Scholar]
  21. 21.
    Edwards TL, Jolly JK, Groppe M, Barnard AR, Cottriall CL et al. 2016. Visual acuity after retinal gene therapy for choroideremia. N. Engl. J. Med. 374:1996–98
     [Google Scholar]
  22. 22.
    Eiraku M, Takata N, Ishibashi H, Kawada M, Sakakura E et al. 2011. Self-organizing optic-cup morphogenesis in three-dimensional culture. Nature 472:51–56
     [Google Scholar]
  23. 23.
    Evans MJ, Kaufman MH. 1981. Establishment in culture of pluripotential cells from mouse embryos. Nature 292:154–56
     [Google Scholar]
  24. 24.
    Farjo R, Skaggs J, Quiambao AB, Cooper MJ, Naash MI 2006. Efficient non-viral ocular gene transfer with compacted DNA nanoparticles. PLOS ONE 1:e38
     [Google Scholar]
  25. 25.
    Fischer AJ, Reh TA. 2001. Müller glia are a potential source of neural regeneration in the postnatal chicken retina. Nat. Neurosci. 4:247–52
     [Google Scholar]
  26. 26.
    Frasson M, Picaud S, Leveillard T, Simonutti M, Mohand-Said S et al. 1999. Glial cell line-derived neurotrophic factor induces histologic and functional protection of rod photoreceptors in the rd/rd mouse. Investig. Ophthalmol. Vis. Sci. 40:2724–34
     [Google Scholar]
  27. 27.
    Fritsche LG, Igl W, Bailey JN, Grassmann F, Sengupta S et al. 2016. A large genome-wide association study of age-related macular degeneration highlights contributions of rare and common variants. Nat. Genet. 48:134–43
     [Google Scholar]
  28. 28.
    Gagliardi G, Ben M'Barek K, Chaffiol A, Slembrouck-Brec A, Conart JB et al. 2018. Characterization and transplantation of CD73-positive photoreceptors isolated from human iPSC-derived retinal organoids. Stem Cell Rep 11:665–80
     [Google Scholar]
  29. 29.
    Garanto A, Chung DC, Duijkers L, Corral-Serrano JC, Messchaert M et al. 2016. In vitro and in vivo rescue of aberrant splicing in CEP290-associated LCA by antisense oligonucleotide delivery. Hum. Mol. Genet. 25:2552–63
     [Google Scholar]
  30. 30.
    Ghazi NG, Abboud EB, Nowilaty SR, Alkuraya H, Alhommadi A et al. 2016. Treatment of retinitis pigmentosa due to MERTK mutations by ocular subretinal injection of adeno-associated virus gene vector: results of a phase I trial. Hum. Genet. 135:327–43
     [Google Scholar]
  31. 31.
    Greenberg KP, Pham A, Werblin FS 2011. Differential targeting of optical neuromodulators to ganglion cell soma and dendrites allows dynamic control of center-surround antagonism. Neuron 69:713–20
     [Google Scholar]
  32. 32.
    Gu SM, Thompson DA, Srikumari CR, Lorenz B, Finckh U et al. 1997. Mutations in RPE65 cause autosomal recessive childhood-onset severe retinal dystrophy. Nat. Genet. 17:194–97
     [Google Scholar]
  33. 33.
    Guziewicz KE, Cideciyan AV, Beltran WA, Komaromy AM, Dufour VL et al. 2018. BEST1 gene therapy corrects a diffuse retina-wide microdetachment modulated by light exposure. PNAS 115:E2839–48
     [Google Scholar]
  34. 34.
    Hageman GS, Anderson DH, Johnson LV, Hancox LS, Taiber AJ et al. 2005. A common haplotype in the complement regulatory gene factor H (HF1/CFH) predisposes individuals to age-related macular degeneration. PNAS 102:7227–32
     [Google Scholar]
  35. 35.
    Haruta M, Sasai Y, Kawasaki H, Amemiya K, Ooto S et al. 2004. In vitro and in vivo characterization of pigment epithelial cells differentiated from primate embryonic stem cells. Investig. Ophthalmol. Vis. Sci. 45:1020–25
     [Google Scholar]
  36. 36.
    Hauswirth WW, Aleman TS, Kaushal S, Cideciyan AV, Schwartz SB et al. 2008. Treatment of Leber congenital amaurosis due to RPE65 mutations by ocular subretinal injection of adeno-associated virus gene vector: short-term results of a phase I trial. Hum. Gene Ther. 19:979–90
     [Google Scholar]
  37. 37.
    Imanishi Y, Batten ML, Piston DW, Baehr W, Palczewski K 2004. Noninvasive two-photon imaging reveals retinyl ester storage structures in the eye. J. Cell Biol. 164:373–83
     [Google Scholar]
  38. 38.
    Iraha S, Tu HY, Yamasaki S, Kagawa T, Goto M et al. 2018. Establishment of immunodeficient retinal degeneration model mice and functional maturation of human ESC-derived retinal sheets after transplantation. Stem Cell Rep 10:1059–74
     [Google Scholar]
  39. 39.
    Ishino Y, Shinagawa H, Makino K, Amemura M, Nakata A 1987. Nucleotide sequence of the iap gene, responsible for alkaline phosphatase isozyme conversion in Escherichia coli, and identification of the gene product. J. Bacteriol. 169:5429–33
     [Google Scholar]
  40. 40.
    Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E 2012. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337:816–21
     [Google Scholar]
  41. 41.
    Jorstad NL, Wilken MS, Grimes WN, Wohl SG, VandenBosch LS et al. 2017. Stimulation of functional neuronal regeneration from Müller glia in adult mice. Nature 548:103–7
     [Google Scholar]
  42. 42.
    Kawasaki H, Suemori H, Mizuseki K, Watanabe K, Urano F et al. 2002. Generation of dopaminergic neurons and pigmented epithelia from primate ES cells by stromal cell-derived inducing activity. PNAS 99:1580–85
     [Google Scholar]
  43. 43.
    Kimberling WJ, Weston MD, Moller C, van Aarem A, Cremers CW et al. 1995. Gene mapping of Usher syndrome type IIa: localization of the gene to a 2.1-cM segment on chromosome 1q41. Am. J. Hum. Genet. 56:216–23
     [Google Scholar]
  44. 44.
    Klein RJ, Zeiss C, Chew EY, Tsai JY, Sackler RS et al. 2005. Complement factor H polymorphism in age-related macular degeneration. Science 308:385–89
     [Google Scholar]
  45. 45.
    Kolomeyer AM, Zarbin MA. 2014. Trophic factors in the pathogenesis and therapy for retinal degenerative diseases. Surv. Ophthalmol. 59:134–65
     [Google Scholar]
  46. 46.
    Lab. Mol. Diagn. Inherit. Eye Dis 2019. RetNet Updated Jan. 9. https://sph.uth.edu/RETNET
  47. 47.
    Lakowski J, Gonzalez-Cordero A, West EL, Han YT, Welby E et al. 2015. Transplantation of photoreceptor precursors isolated via a cell surface biomarker panel from embryonic stem cell-derived self-forming retina. Stem Cells 33:2469–82
     [Google Scholar]
  48. 48.
    Leveillard T, Mohand-Said S, Lorentz O, Hicks D, Fintz AC et al. 2004. Identification and characterization of rod-derived cone viability factor. Nat. Genet. 36:755–59
     [Google Scholar]
  49. 49.
    Lin JY, Knutsen PM, Muller A, Kleinfeld D, Tsien RY 2013. ReaChR: a red-shifted variant of channelrhodopsin enables deep transcranial optogenetic excitation. Nat. Neurosci. 16:1499–508
     [Google Scholar]
  50. 50.
    MacLaren RE, Pearson RA, MacNeil A, Douglas RH, Salt TE et al. 2006. Retinal repair by transplantation of photoreceptor precursors. Nature 444:203–7
     [Google Scholar]
  51. 51.
    Maeda A, Palczewska G, Golczak M, Kohno H, Dong Z et al. 2014. Two-photon microscopy reveals early rod photoreceptor cell damage in light-exposed mutant mice. PNAS 111:E1428–37
     [Google Scholar]
  52. 52.
    Maguire AM, Simonelli F, Pierce EA, Pugh EN Jr., Mingozzi F et al. 2008. Safety and efficacy of gene transfer for Leber's congenital amaurosis. N. Engl. J. Med. 358:2240–48
     [Google Scholar]
  53. 53.
    Mandai M, Fujii M, Hashiguchi T, Sunagawa GA, Ito SI et al. 2017. iPSC-derived retina transplants improve vision in rd1 end-stage retinal-degeneration mice. Stem Cell Rep 8:69–83
     [Google Scholar]
  54. 54.
    Mandai M, Kurimoto Y, Takahashi M 2017. Autologous induced stem-cell-derived retinal cells for macular degeneration. N. Engl. J. Med. 377:792–93
     [Google Scholar]
  55. 55.
    Mehat MS, Sundaram V, Ripamonti C, Robson AG, Smith AJ et al. 2018. Transplantation of human embryonic stem cell-derived retinal pigment epithelial cells in macular degeneration. Ophthalmology 125:1765–75
     [Google Scholar]
  56. 56.
    Mihelec M, Pearson RA, Robbie SJ, Buch PK, Azam SA et al. 2011. Long-term preservation of cones and improvement in visual function following gene therapy in a mouse model of Leber congenital amaurosis caused by guanylate cyclase-1 deficiency. Hum. Gene Ther. 22:1179–90
     [Google Scholar]
  57. 57.
    Miyazaki M, Ikeda Y, Yonemitsu Y, Goto Y, Kohno R et al. 2008. Synergistic neuroprotective effect via simian lentiviral vector-mediated simultaneous gene transfer of human pigment epithelium-derived factor and human fibroblast growth factor-2 in rodent models of retinitis pigmentosa. J. Gene Med. 10:1273–81
     [Google Scholar]
  58. 58.
    Murakami Y, Ikeda Y, Yonemitsu Y, Onimaru M, Nakagawa K et al. 2008. Inhibition of nuclear translocation of apoptosis-inducing factor is an essential mechanism of the neuroprotective activity of pigment epithelium-derived factor in a rat model of retinal degeneration. Am. J. Pathol. 173:1326–38
     [Google Scholar]
  59. 59.
    Nagel G, Brauner M, Liewald JF, Adeishvili N, Bamberg E, Gottschalk A 2005. Light activation of channelrhodopsin-2 in excitable cells of Caenorhabditis elegans triggers rapid behavioral responses. Curr. Biol. 15:2279–84
     [Google Scholar]
  60. 60.
    Nagel G, Ollig D, Fuhrmann M, Kateriya S, Musti AM et al. 2002. Channelrhodopsin-1: a light-gated proton channel in green algae. Science 296:2395–98
     [Google Scholar]
  61. 61.
    Nakano T, Ando S, Takata N, Kawada M, Muguruma K et al. 2012. Self-formation of optic cups and storable stratified neural retina from human ESCs. Cell Stem Cell 10:771–85
     [Google Scholar]
  62. 62.
    Oishi M, Oishi A, Gotoh N, Ogino K, Higasa K et al. 2014. Comprehensive molecular diagnosis of a large cohort of Japanese retinitis pigmentosa and Usher syndrome patients by next-generation sequencing. Investig. Ophthalmol. Vis. Sci. 55:7369–75
     [Google Scholar]
  63. 63.
    Okoye G, Zimmer J, Sung J, Gehlbach P, Deering T et al. 2003. Increased expression of brain-derived neurotrophic factor preserves retinal function and slows cell death from rhodopsin mutation or oxidative damage. J. Neurosci. 23:4164–72
     [Google Scholar]
  64. 64.
    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 101:13654–59
     [Google Scholar]
  65. 65.
    Osakada F, Ikeda H, Mandai M, Wataya T, Watanabe K et al. 2008. Toward the generation of rod and cone photoreceptors from mouse, monkey and human embryonic stem cells. Nat. Biotechnol. 26:215–24
     [Google Scholar]
  66. 66.
    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. 27:4210–19
     [Google Scholar]
  67. 67.
    Palczewska G, Maeda T, Imanishi Y, Sun W, Chen Y et al. 2010. Noninvasive multiphoton fluorescence microscopy resolves retinol and retinal condensation products in mouse eyes. Nat. Med. 16:1444–49
     [Google Scholar]
  68. 68.
    Palczewski K, Kumasaka T, Hori T, Behnke CA, Motoshima H et al. 2000. Crystal structure of rhodopsin: a G protein-coupled receptor. Science 289:739–45
     [Google Scholar]
  69. 69.
    Pearson RA, Barber AC, Rizzi M, Hippert C, Xue T et al. 2012. Restoration of vision after transplantation of photoreceptors. Nature 485:99–103
     [Google Scholar]
  70. 70.
    Pearson RA, Gonzalez-Cordero A, West EL, Ribeiro JR, Aghaizu N et al. 2016. Donor and host photoreceptors engage in material transfer following transplantation of post-mitotic photoreceptor precursors. Nat. Commun. 7:13029
     [Google Scholar]
  71. 71.
    Redmond TM, Yu S, Lee E, Bok D, Hamasaki D et al. 1998. Rpe65 is necessary for production of 11-cis-vitamin A in the retinal visual cycle. Nat. Genet. 20:344–51
     [Google Scholar]
  72. 72.
    Roorda A, Duncan JL. 2015. Adaptive optics ophthalmoscopy. Annu. Rev. Vis. Sci. 1:19–50
     [Google Scholar]
  73. 73.
    Sagdullaev BT, Aramant RB, Seiler MJ, Woch G, McCall MA 2003. Retinal transplantation-induced recovery of retinotectal visual function in a rodent model of retinitis pigmentosa. Investig. Ophthalmol. Vis. Sci. 44:1686–95
     [Google Scholar]
  74. 74.
    Santos-Ferreira T, Llonch S, Borsch O, Postel K, Haas J, Ader M 2016. Retinal transplantation of photoreceptors results in donor-host cytoplasmic exchange. Nat. Commun. 7:13028
     [Google Scholar]
  75. 75.
    Schwartz SD, Hubschman JP, Heilwell G, Franco-Cardenas V, Pan CK et al. 2012. Embryonic stem cell trials for macular degeneration: a preliminary report. Lancet 379:713–20
     [Google Scholar]
  76. 76.
    Schwartz SD, Regillo CD, Lam BL, Eliott D, Rosenfeld PJ et al. 2015. Human embryonic stem cell-derived retinal pigment epithelium in patients with age-related macular degeneration and Stargardt's macular dystrophy: follow-up of two open-label phase 1/2 studies. Lancet 385:509–16
     [Google Scholar]
  77. 77.
    Sengupta A, Chaffiol A, Mace E, Caplette R, Desrosiers M et al. 2016. Red-shifted channelrhodopsin stimulation restores light responses in blind mice, macaque retina, and human retina. EMBO Mol. Med. 8:1248–64
     [Google Scholar]
  78. 78.
    Shirai H, Mandai M, Matsushita K, Kuwahara A, Yonemura S et al. 2016. Transplantation of human embryonic stem cell-derived retinal tissue in two primate models of retinal degeneration. PNAS 113:E81–90
     [Google Scholar]
  79. 79.
    Singh MS, Balmer J, Barnard AR, Aslam SA, Moralli D et al. 2016. Transplanted photoreceptor precursors transfer proteins to host photoreceptors by a mechanism of cytoplasmic fusion. Nat. Commun. 7:13537
     [Google Scholar]
  80. 80.
    Singh MS, Charbel Issa P, Butler R, Martin C, Lipinski DM et al. 2013. Reversal of end-stage retinal degeneration and restoration of visual function by photoreceptor transplantation. PNAS 110:1101–6
     [Google Scholar]
  81. 81.
    Stone EM, Aldave AJ, Drack AV, Maccumber MW, Sheffield VC et al. 2012. Recommendations for genetic testing of inherited eye diseases: report of the American Academy of Ophthalmology task force on genetic testing. Ophthalmology 119:2408–10
     [Google Scholar]
  82. 82.
    Sugita S, Iwasaki Y, Makabe K, Kamao H, Mandai M et al. 2016. Successful transplantation of retinal pigment epithelial cells from MHC homozygote iPSCs in MHC-matched models. Stem Cell Rep 7:635–48
     [Google Scholar]
  83. 83.
    Sugita S, Iwasaki Y, Makabe K, Kimura T, Futagami T et al. 2016. Lack of T cell response to iPSC-derived retinal pigment epithelial cells from HLA homozygous donors. Stem Cell Rep 7:619–34
     [Google Scholar]
  84. 84.
    Sun D, Sahu B, Gao S, Schur RM, Vaidya AM et al. 2017. Targeted multifunctional lipid ECO plasmid DNA nanoparticles as efficient non-viral gene therapy for Leber's congenital amaurosis. Mol. Ther. Nucleic Acids 7:42–52
     [Google Scholar]
  85. 85.
    Takahashi K, Yamanaka S. 2006. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663–76
     [Google Scholar]
  86. 86.
    Tomita H, Sugano E, Isago H, Hiroi T, Wang Z et al. 2010. Channelrhodopsin-2 gene transduced into retinal ganglion cells restores functional vision in genetically blind rats. Exp. Eye Res. 90:429–36
     [Google Scholar]
  87. 87.
    Tomita H, Sugano E, Murayama N, Ozaki T, Nishiyama F et al. 2014. Restoration of the majority of the visual spectrum by using modified Volvox channelrhodopsin-1. Mol. Ther. 22:1434–40
     [Google Scholar]
  88. 88.
    Tu HY, Watanabe T, Shirai H, Yamasaki S, Kinoshita M 2019. Medium- to long-term survival and functional examination of human iPSC-derived retinas in rat and primate models of retinal degeneration. EBioMedicine 39:562–74
     [Google Scholar]
  89. 89.
    van Zeeburg EJ, Maaijwee KJ, Missotten TO, Heimann H, van Meurs JC 2012. A free retinal pigment epithelium–choroid graft in patients with exudative age-related macular degeneration: results up to 7 years. Am. J. Ophthalmol. 153:120–27.e2
     [Google Scholar]
  90. 90.
    Verbakel SK, van Huet RAC, Boon CJF, den Hollander AI, Collin RWJ et al. 2018. Non-syndromic retinitis pigmentosa. Prog. Retin. Eye Res. 66:157–86
     [Google Scholar]
  91. 91.
    Williams DR. 2011. Imaging single cells in the living retina. Vis. Res. 51:1379–96
     [Google Scholar]
  92. 92.
    Woch G, Aramant RB, Seiler MJ, Sagdullaev BT, McCall MA 2001. Retinal transplants restore visually evoked responses in rats with photoreceptor degeneration. Investig. Ophthalmol. Vis. Sci. 42:1669–76
     [Google Scholar]
  93. 93.
    Yao K, Qiu S, Wang YV, Park SJH, Mohns EJ et al. 2018. Restoration of vision after de novo genesis of rod photoreceptors in mammalian retinas. Nature 560:484–88
     [Google Scholar]
  94. 94.
    Zhang F, Prigge M, Beyriere F, Tsunoda SP, Mattis J et al. 2008. Red-shifted optogenetic excitation: a tool for fast neural control derived from Volvox carteri. Nat. . Neurosci 11:631–33
     [Google Scholar]
  95. 95.
    Zulliger R, Conley SM, Naash MI 2015. Non-viral therapeutic approaches to ocular diseases: an overview and future directions. J. Control. Release 219:471–87
     [Google Scholar]
/content/journals/10.1146/annurev-genom-083118-015043
Loading
Gene and Induced Pluripotent Stem Cell Therapy for Retinal Diseases
Annual Review of Genomics and Human Genetics 20, 201 (2019); https://doi.org/10.1146/annurev-genom-083118-015043
/content/journals/10.1146/annurev-genom-083118-015043
/content/journals/10.1146/annurev-genom-083118-015043
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error