1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Vision Science
  4. Volume 3, 2017
  5. Article

Annual Review of Vision Science

Volume 3, 2017

Vectors and Gene Delivery to the Retina

Abstract

One of the great advantages of the retina as a target tissue for gene delivery is the wide array of genetic tools that have been developed in the past decade. This includes a variety of vectors for therapeutic gene delivery to most types of retinal neurons and glia, as well as cell type–specific promoters for restricted gene expression in distinct neuronal subtypes. Within the scope of neuroscience applications and for gene therapy, it is now routine to express reporter genes, replacement genes, neuronal activity indicators, and microbial opsins in specific neuronal types in the mouse retina. However, there are considerable anatomical, physiological, immunological, and behavioral differences between the mouse and the human that limit the usefulness of these tools in humans and nonhuman primates. Several advances are now being made toward the goal of applying viral targeting tools to understand the primate retina. Here, we describe these advances, consider their potential to advance our understanding of the primate retina, and describe what will be needed to move forward.

Keyword(s): adeno-associated virus, adenovirus, directed evolution, lentivirus, miRNA, nanoparticles, optogenetics, promoter
Loading

Article metrics loading...

/content/journals/10.1146/annurev-vision-102016-061413
2017-09-15
2024-05-09
Loading full text...

Full text loading...

/deliver/fulltext/vision/3/1/annurev-vision-102016-061413.html?itemId=/content/journals/10.1146/annurev-vision-102016-061413&mimeType=html&fmt=ahah

Literature Cited

  1. Acland GM, Aguirre GD, Bennett J, Aleman TS, Cideciyan AV. et al. 2005. Long-term restoration of rod and cone vision by single dose rAAV-mediated gene transfer to the retina in a canine model of childhood blindness. Mol. Ther. 12:61072–82 [Google Scholar]
  2. Adijanto J, Naash MI. 2015. Nanoparticle-based technologies for retinal gene therapy. Eur. J. Pharm. Biopharm. 95:B353–67 [Google Scholar]
  3. Alexander JJ, Hauswirth WW. 2008. Adeno-associated viral vectors and the retina. Recent Advances in Retinal Degeneration RE Anderson, MM LaVail, JG Hollyfield 121–28 Adv. Exp. Med. Biol 613 New York: Springer [Google Scholar]
  4. Alexander JJ, Umino Y, Everhart D, Chang B, Min SH. et al. 2007. Restoration of cone vision in a mouse model of achromatopsia. Nat. Med. 13:6685–87 [Google Scholar]
  5. Allocca M, Mussolino C, Garcia-Hoyos M, Sanges D, Iodice C. et al. 2007. Novel adeno-associated virus serotypes efficiently transduce murine photoreceptors. J. Virol. 81:2011372–80 [Google Scholar]
  6. Apaolaza PS, del Pozo-Rodríguez A, Solinís MA, Rodríguez JM, Friedrich U. et al. 2016. Structural recovery of the retina in a retinoschisin-deficient mouse after gene replacement therapy by solid lipid nanoparticles. Biomaterials 90:40–49 [Google Scholar]
  7. Auricchio A, Behling KC, Maguire AM, O'Conner EE, Bennett J. et al. 2002. Inhibition of retinal neovascularization by intraocular viral-mediated delivery of anti-angiogenic agents. Mol. Ther. 6:4490–94 [Google Scholar]
  8. Auricchio A, Kobinger G, Anand V, Hildinger M, O'Conner E. et al. 2001. Exchange of surface proteins impacts on viral vector cellular specificity and transduction characteristics: the retina as a model. Hum. Mol. Genet. 10:263075–81 [Google Scholar]
  9. Battaglia L, Serpe L, Foglietta F, Muntoni E, Gallarate M. et al. 2016. Application of lipid nanoparticles to ocular drug delivery application of lipid nanoparticles to ocular drug delivery. Expert Opin. Drug Deliv. 13:121743–57 [Google Scholar]
  10. Belmonte JCI, Callaway EM, Churchland P, Caddick SJ, Feng G. et al. 2015. Brains, genes, and primates. Neuron 86:3617–31 [Google Scholar]
  11. Boye SE, Alexander JJ, Boye SL, Witherspoon CD, Sandefer KJ. et al. 2012. The human rhodopsin kinase promoter in an AAV5 vector confers rod- and cone-specific expression in the primate retina. Hum. Gene Ther. 23:101101–15 [Google Scholar]
  12. Boye SE, Alexander JJ, Witherspoon CD, Boye SL, Peterson JJ. et al. 2016. Highly efficient delivery of adeno-associated viral vectors to the primate retina. Hum. Gene Ther. 27:8580–97 [Google Scholar]
  13. Boye SE, Boye SL, Pang J, Ryals R, Everhart D. et al. 2010. Functional and behavioral restoration of vision by gene therapy in the guanylate cyclase-1 (GC1) knockout mouse. PLOS ONE 5:6e11306 [Google Scholar]
  14. Busskamp V, Duebel J, Balya D, Fradot M, Viney TJ. et al. 2010. Genetic reactivation of cone photoreceptors restores visual responses in retinitis pigmentosa. Science 329:5990413–17 [Google Scholar]
  15. Busskamp V, Roska B. 2011. Optogenetic approaches to restoring visual function in retinitis pigmentosa. Curr. Opin. Neurobiol. 21:6942–46 [Google Scholar]
  16. Byrne LC, Dalkara D, Luna G, Fisher SK, Clérin E. et al. 2015a. Viral-mediated RdCVF and RdCVFL expression protects cone and rod photoreceptors in retinal degeneration. J. Clin. Investig. 125:1105–16 [Google Scholar]
  17. Byrne LC, Lin YJ, Lee T, Schaffer D V, Flannery JG. 2015b. The expression pattern of systemically injected AAV9 in the developing mouse retina is determined by age. Mol. Ther. 23:2290–96 [Google Scholar]
  18. Callaway EM. 2008. Transneuronal circuit tracing with neurotropic viruses. Curr. Opin. Neurobiol. 18:6617–23 [Google Scholar]
  19. 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. 19:71212–19 [Google Scholar]
  20. Castle MJ, Turunen HT, Vandenberghe LH, Wolfe JH. 2016. Controlling AAV tropism in the nervous system with natural and engineered capsids. Gene Therapy for Neurological Disorders FP Manfredsson 133–49 Meth. Mol. Biol. 1382 New York: Springer [Google Scholar]
  21. Cearley CN, Wolfe JH. 2006. Transduction characteristics of adeno-associated virus vectors expressing cap serotypes 7, 8, 9, and Rh10 in the mouse brain. Mol. Ther. 13:3528–37 [Google Scholar]
  22. Cehajic-Kapetanovic J, Le Goff MM, Allen A, Lucas RJ, Bishop PN. 2011. Glycosidic enzymes enhance retinal transduction following intravitreal delivery of AAV2. Mol. Vis. 17:1771–83 [Google Scholar]
  23. Colella P, Trapani I, Cesi G, Sommella A, Manfredi A. et al. 2014. Efficient gene delivery to the cone-enriched pig retina by dual AAV vectors. Gene Ther 21:4450–56 [Google Scholar]
  24. Comander J, Carvalho LS, Xiao R, Langsdorf A, Wassmer S. et al. 2016. Characterization of the limitations to gene transfer and associated inflammation following intravitreal AAV injection in nonhuman primates. ARVO 57:771 [Google Scholar]
  25. Conlon TJ, Deng W-T, Erger K, Cossette T, Pang J-j. et al. 2013. Preclinical potency and safety studies of an AAV2-mediated gene therapy vector for the treatment of MERTK associated retinitis pigmentosa. Hum. Gene Ther. Clin. Dev. 24:123–28 [Google Scholar]
  26. Cronin T, Vandenberghe LH, Hantz P, Juttner J, Reimann A. et al. 2014. Efficient transduction and optogenetic stimulation of retinal bipolar cells by a synthetic adeno-associated virus capsid and promoter. EMBO Mol. Med. 6:91175–90 [Google Scholar]
  27. Dalkara D, Byrne LC, Klimczak RR, Visel M, Yin L. et al. 2013. In vivo-directed evolution of a new adeno-associated virus for therapeutic outer retinal gene delivery from the vitreous. Sci. Transl. Med. 5:189189ra76 [Google Scholar]
  28. Dalkara D, Byrne LC, Lee T, Hoffmann NV, Schaffer DV, Flannery JG. 2012. Enhanced gene delivery to the neonatal retina through systemic administration of tyrosine-mutated AAV9. Gene Ther 19:176–81 [Google Scholar]
  29. Dalkara D, Kolstad KD, Caporale N, Visel M, Klimczak RR. et al. 2009. Inner limiting membrane barriers to AAV-mediated retinal transduction from the vitreous. Mol. Ther. 17:122096–102 [Google Scholar]
  30. de Leeuw CN, Dyka FM, Boye SL, Laprise S, Zhou M. et al. 2014. Targeted CNS delivery using human MiniPromoters and demonstrated compatibility with adeno-associated viral vectors. Mol. Ther. Methods Clin. Dev. 1:5 [Google Scholar]
  31. Doroudchi MM, Greenberg KP, Liu J, Silka KA, Boyden ES. et al. 2011. Virally delivered channelrhodopsin-2 safely and effectively restores visual function in multiple mouse models of blindness. Mol. Ther. 19:71220–29 [Google Scholar]
  32. Dorrell MI, Aguilar E, Jacobson R, Yanes O, Gariano R. et al. 2009. Antioxidant or neurotrophic factor treatment preserves function in a mouse model of neovascularization-associated oxidative stress. J. Clin. Investig. 119:3611–23 [Google Scholar]
  33. Dudus L, Anand V, Acland GM, Chen S-J, Wilson JM. et al. 1999. Persistent transgene product in retina, optic nerve and brain after intraocular injection of rAAV. Vis. Res. 39:152545–53 [Google Scholar]
  34. Dum RP, Strick PL. 2013. Transneuronal tracing with neurotropic viruses reveals network macroarchitecture Curr. Opin. . Neurobiol. 23:2245–49 [Google Scholar]
  35. Dyka FM, Boye SL, Ryals RC, Chiodo VA, Boye SE, Hauswirth WW. 2014. Cone specific promoter for use in gene therapy of retinal degenerative diseases. Retinal Degenerative Diseases J Ash, C Grimm, J Hollyfield, R Anderson, M LaVail, C Bowes Rickman 695–701 Adv. Exp. Med. Biol 801 New York: Springer [Google Scholar]
  36. El-Shamayleh Y, Ni AM, Horwitz GD. 2016. Strategies for targeting primate neural circuits with viral vectors. J. Neurophysiol. 116:122–34 [Google Scholar]
  37. Farjo R, Skaggs J, Quiambao AB, Cooper MJ, Naash MI. 2006. Efficient non-viral ocular gene transfer with compacted DNA nanoparticles. PLOS ONE 1:1e38 [Google Scholar]
  38. Fink TL, Klepcyk PJ, Oette SM, Gedeon CR, Hyatt SL. et al. 2006. Plasmid size up to 20 kbp does not limit effective in vivo lung gene transfer using compacted DNA nanoparticles. Gene Ther 13:131048–51 [Google Scholar]
  39. Flannery JG, Zolotukhin S, Vaquero MI, LaVail MM, Muzyczka N. et al. 1997. Efficient photoreceptor-targeted gene expression in vivo by recombinant adeno-associated virus. PNAS 94:136916–21 [Google Scholar]
  40. Gaub BM, Berry MH, Holt AE, Isacoff EY, Flannery JG. 2015. Optogenetic vision restoration using rhodopsin for enhanced sensitivity. Mol. Ther. 23:101562–71 [Google Scholar]
  41. Glushakova LG, Timmers AM, Pang J, Teusner JT, Hauswirth WW. 2006. Human blue-opsin promoter preferentially targets reporter gene expression to rat S-cone photoreceptors. Investig. Opthalmol. Vis. Sci. 47:83505 [Google Scholar]
  42. Granstedt AE, Szpara ML, Kuhn B, Wang SSH, Enquist LW. 2009. Fluorescence-based monitoring of in vivo neural activity using a circuit-tracing pseudorabies virus. PLOS ONE 4:9e6923 [Google Scholar]
  43. Guy J, Qi X, Wang H, Hauswirth WW. 1999. Adenoviral gene therapy with catalase suppresses experimental optic neuritis. Arch. Ophthalmol. 117:111533–39 [Google Scholar]
  44. Guziewicz KE, Zangeri B, Komáromy A, Iwabe S, Chiodo VA, Boye SL. 2013. Recombinant AAV-mediated BEST1 transfer to the retinal pigment epithelium: analysis of serotype-dependent retinal effects. PLOS ONE 8:10e75666 [Google Scholar]
  45. Han Z, Conley SM, Makkia RS, Cooper MJ, Naash MI. 2012a. DNA nanoparticle-mediated ABCA4 delivery rescues Stargardt dystrophy in mice. J. Clin. Investig. 122:93221–26 [Google Scholar]
  46. Han Z, Conley SM, Makkia R, Guo J, Cooper MJ, Naash MI. 2012b. Comparative analysis of DNA nanoparticles and AAVs for ocular gene delivery. PLOS ONE 7:12e52189 [Google Scholar]
  47. Heintz N. 2001. BAC to the future: the use of bac transgenic mice for neuroscience research. Nat. Rev. Neurosci. 2:12861–70 [Google Scholar]
  48. Hellström M, Ruitenberg MJ, Pollett MA, Ehlert EME, Twisk J. et al. 2009. Cellular tropism and transduction properties of seven adeno-associated viral vector serotypes in adult retina after intravitreal injection. Gene Ther 16:521–32 [Google Scholar]
  49. Huberman AD, Manu M, Koch SM, Susman MW, Lutz AB. et al. 2008. Architecture and activity-mediated refinement of axonal projections from a mosaic of genetically identified retinal ganglion cells. Neuron 59:3425–38 [Google Scholar]
  50. Huberman AD, Wei W, Elstrott J, Stafford BK, Feller MB, Barres BA. 2009. Genetic identification of an On-Off direction- selective retinal ganglion cell subtype reveals a layer-specific subcortical map of posterior motion. Neuron 62:3327–34 [Google Scholar]
  51. Inatani M, Tanihara H. 2002. Proteoglycans in retina. Prog. Retin. Eye Res. 21:5429–47 [Google Scholar]
  52. Ivanova E, Hwang G-S, Pan Z-H, Troilo D. 2010. Evaluation of AAV-mediated expression of Chop2-GFP in the marmoset retina. Investig. Ophthalmol. Vis. Sci. 51:105288–96 [Google Scholar]
  53. Kay CN, Ryals RC, Aslanidi GV, Min SH, Ruan Q. et al. 2013. Targeting photoreceptors via intravitreal delivery using novel, capsid-mutated AAV vectors. PLOS ONE 8:4e62097 [Google Scholar]
  54. Kay MA, Glorioso JC, Naldini L. 2001. Viral vectors for gene therapy: the art of turning infectious agents into vehicles of therapeutics. Nat. Med. 7:33–40 [Google Scholar]
  55. Khani SC, Pawlyk BS, Bulgakov OV, Kasperek E, Young JE. et al. 2007. AAV-mediated expression targeting of rod and cone photoreceptors with a human rhodopsin kinase promoter. Investig. Opthalmol. Vis. Sci. 48:93954 [Google Scholar]
  56. Klimczak RR, Koerber JT, Dalkara D, Flannery JG, Schaffer DV. 2009. A novel adeno-associated viral variant for efficient and selective intravitreal transduction of rat Müller cells. PLOS ONE 4:10e7467 [Google Scholar]
  57. Koerber JT, Klimczak R, Jang J-H, Dalkara D, Flannery JG, Schaffer DV. 2009. Molecular evolution of adeno-associated virus for enhanced glial gene delivery. Mol. Ther. 17:122088–95 [Google Scholar]
  58. Koilkonda RD, Guy J. 2011. Leber's hereditary optic neuropathy-gene therapy: from benchtop to bedside. J. Ophthalmol. 2011:179412 [Google Scholar]
  59. Koirala A, Makkia RS, Conley SM, Cooper MJ, Naash MI. 2013. S/MAR-containing DNA nanoparticles promote persistent RPE gene expression and improvement in RPE65-associated LCA. Hum. Mol. Genet. 22:81632–42 [Google Scholar]
  60. Kolstad KD, Dalkara D, Guerin K, Visel M, Hoffmann N. et al. 2010. Changes in adeno-associated virus-mediated gene delivery in retinal degeneration. Hum. Gene Ther. 21:5571–78 [Google Scholar]
  61. Komáromy AM, Alexander JJ, Rowlan JS, Garcia MM, Chiodo VA. et al. 2010. Gene therapy rescues cone function in congenital achromatopsia. Hum. Mol. Genet. 19:2581–93 [Google Scholar]
  62. Kotterman MA, Schaffer DV. 2014. Engineering adeno-associated viruses for clinical gene therapy. Nat. Rev. Genet. 15:7445–51 [Google Scholar]
  63. Kotterman MA, Yin L, Strazzeri JM, Flannery JG, Merigan WH, Schaffer DV. 2014. Antibody neutralization poses a barrier to intravitreal adeno-associated viral vector gene delivery to non-human primates. Gene Ther 22:2116–26 [Google Scholar]
  64. Kwon I, Schaffer DV. 2008. Designer gene delivery vectors: molecular engineering and evolution of adeno-associated viral vectors for enhanced gene transfer. Pharm. Res. 25:3489–99 [Google Scholar]
  65. Lau D, McGee LH, Zhou S, Rendahl KG, Manning WC. et al. 2000. Retinal degeneration is slowed in transgenic rats by AAV-mediated delivery of FGF-2. Investig. Ophthalmol. Vis. Sci. 41:113622–33 [Google Scholar]
  66. Le Meur G, Stieger K, Smith AJ, Weber M, Deschamps JY. et al. 2007. Restoration of vision in RPE65-deficient Briard dogs using an AAV serotype 4 vector that specifically targets the retinal pigmented epithelium. Gene Ther 14:4292–303 [Google Scholar]
  67. Li Q, Timmers AM, Guy J, Pang J, Hauswirth WW. 2008. Cone-specific expression using a human red opsin promoter in recombinant AAV. Vis. Res. 48:3332–38 [Google Scholar]
  68. Lin JY, Lin MZ, Steinbach P, Tsien RY. 2009. Characterization of engineered channelrhodopsin variants with improved properties and kinetics. Biophys. J. 96:51803–14 [Google Scholar]
  69. Lipinski DM, Thake M, MacLaren RE. 2013. Clinical applications of retinal gene therapy. Prog. Retin. Eye Res. 32:22–47 [Google Scholar]
  70. Liu J, Timmers AM, Lewin AS, Hauswirth. 2005. Ribozyme knockdown of the γ-subunit of rod cGMP phosphodiesterase alters the ERG and retinal morphology in wild-type mice. Investig. Ophthalmol. Vis. Sci. 46:103836–44 [Google Scholar]
  71. Lu Q, Ganjawala TH, Ivanova E, Cheng JG, Troilo D, Pan Z-H. 2016. AAV-mediated transduction and targeting of retinal bipolar cells with improved mGluR6 promoters in rodents and primates. Gene Ther 23:680–89 [Google Scholar]
  72. Macé E, Caplette R, Marre O, Sengupta A, Chaffiol A. et al. 2015. Targeting channelrhodopsin-2 to ON-bipolar cells with vitreally administered AAV restores ON and OFF visual responses in blind mice. Mol. Ther. 23:17–16 [Google Scholar]
  73. MacLachlan TK, Lukason M, Collins M, Munger R, Isenberger E. et al. 2011. Preclinical safety evaluation of AAV2-sFLT01—a gene therapy for age-related macular degeneration. Mol. Ther. 19:2326–34 [Google Scholar]
  74. Mancuso K, Hauswirth WW, Li Q, Connor TB, Kuchenbecker JA. et al. 2009. Gene therapy for red-green colour blindness in adult primates. Nature 461:7265784–87 [Google Scholar]
  75. Manfredi A, Marrocco E, Agostina P, Giulia C, Sinnekka A. et al. 2013. Combined rod and cone transduction by adeno-associated virus 2/8. Hum. Gene Ther. 24:12982–92 [Google Scholar]
  76. Matsumoto B, Blanks JC, Ryan SJ. 1984. Topographic variations in the rabbit and primate internal limiting membrane. Investig. Ophthalmol. Vis. Sci. 25:71–82 [Google Scholar]
  77. Mazzoni F, Safa H, Finnemann SC. 2014. Understanding photoreceptor outer segment phagocytosis: use and utility of RPE cells in culture. Exp. Eye Res. 126:51–60 [Google Scholar]
  78. McKinnon SJ, Lehman DM, Takzib NG, Ransom NL, Reitsamer HA. et al. 2002. Baculoviral IAP repeat-containing-4 protects optic nerve axons in a rat glaucoma model. Mol. Ther. 5:6780–87 [Google Scholar]
  79. Michalakis S, Mühlfriedel R, Tanimoto N, Krishnamoorthy V, Koch S. et al. 2010. Restoration of cone vision in the CNGA3−/− mouse model of congenital complete lack of cone photoreceptor function. Mol. Ther. 18:122057–63 [Google Scholar]
  80. Mitra RN, Han Z, Merwin M, Al Taai M, Conley SM, Naash MI. 2014. Synthesis and characterization of glycol chitosan DNA nanoparticles for retinal gene delivery. Chem. Med. Chem 91189–96 [Google Scholar]
  81. Mussolino C, della Corte M, Rossi S, Viola F, Di Vicino U. et al. 2011. AAV-mediated photoreceptor transduction of the pig cone-enriched retina. Gene Ther 18:7637–45 [Google Scholar]
  82. Naik R, Mukhopadhyay A, Ganguli M. 2009. Gene delivery to the retina: focus on non-viral approaches. Drug Discov. Today 14:5–6306–15 [Google Scholar]
  83. Packer AM, Roska B, Häusser M. 2013. Targeting neurons and photons for optogenetics. Nat. Neurosci. 16:7805–15 [Google Scholar]
  84. Park TK, Wu Z, Kjellstrom S, Zeng Y, Bush RA. et al. 2009. Intravitreal delivery of AAV8 retinoschisin results in cell type-specific gene expression and retinal rescue in the Rs1-KO mouse. Gene Ther 16:7916–26 [Google Scholar]
  85. Pellissier LP, Quinn PM, Henrique Alves C, Vos RM, Klooster J. et al. 2015. Gene therapy into photoreceptors and Müller glial cells restores retinal structure and function in CRB1 retinitis pigmentosa mouse models. Hum. Mol. Genet. 24:113104–18 [Google Scholar]
  86. Petrs-Silva H, Dinculescu A, Li Q, Deng W-T, Pang J-j. et al. 2011. Novel properties of tyrosine-mutant AAV2 vectors in the mouse retina. Mol. Ther. 19:2293–301 [Google Scholar]
  87. Petrs-Silva H, Dinculescu A, Li Q, Min S-H, Chiodo V. et al. 2009. High-efficiency transduction of the mouse retina by tyrosine-mutant AAV serotype vectors. Mol. Ther. 17:3463–71 [Google Scholar]
  88. Prentice HM, Biswal MR, Dorey K, Blanks JC. 2011. Hypoxia-regulated retinal glial cell-specific promoter for potential gene therapy in disease. Investig. Ophthalmol. Vis. Sci. 52:128562–70 [Google Scholar]
  89. Puras G, Zarate J, Díaz-Tahoces A, Avilés-Trigueros M, Fernández E, Pedraz JL. 2013. Oligochitosan polyplexes as carriers for retinal gene delivery. Eur. J. Pharm. Sci. 48:1–2323–31 [Google Scholar]
  90. Ramachandran P, Lee V, Wei Z, Song JY, Casal G. et al. 2017. Evaluation of dose and safety of AAV7m8 and AAV8BP2 in the non-human primate retina. Hum. Gene Ther. 28:2154–67 [Google Scholar]
  91. Sasaki E, Suemizu H, Shimada A, Hanazawa K, Oiwa R. et al. 2009. Generation of transgenic non-human primates with germline transmission. Nature 459:523–27 [Google Scholar]
  92. Scalabrino ML, Boye SL, Fransen KMH, Noel JM, Dyka FM. et al. 2015. Intravitreal delivery of a novel AAV vector targets ON bipolar cells and restores visual function in a mouse model of complete congenital stationary night blindness. Hum. Mol. Genet. 9342:3521–32 [Google Scholar]
  93. Shen SQ, Myers CA, Hughes AEO, Byrne LC, Flannery JG, Corbo JC. 2016. Massively parallel cis-regulatory analysis in the mammalian central nervous system. Genome Res. 26:238–55 [Google Scholar]
  94. Stieger K, Lhériteau E, Lhéariteau E, Moullier P, Rolling F. 2009. AAV-mediated gene therapy for retinal disorders in large animal models. ILAR J 50:2206–24 [Google Scholar]
  95. Sutanto EN, Zhang D, Lai YKY, Shen W-Y, Rakoczy EP. 2005. Development and evaluation of the specificity of a cathepsin D proximal promoter in the eye. Curr. Eye Res. 30:153–61 [Google Scholar]
  96. Tan MH, Smith AJ, Pawlyk B, Xu X, Liu X. et al. 2009. Gene therapy for retinitis pigmentosa and Leber congenital amaurosis caused by defects in AIPL1: effective rescue of mouse models of partial and complete Aipl1 deficiency using AAV2/2 and AAV2/8 vectors. Hum. Mol. Genet. 18:122099–114 [Google Scholar]
  97. Tang JCY, Rudolph S, Dhande OS, Abraira VE, Choi S. et al. 2015. Cell type–specific manipulation with GFP-dependent Cre recombinase. Nat. Neurosci. 18:91334–41 [Google Scholar]
  98. Tang JCY, Szikra T, Kozorovitskiy Y, Teixiera M, Sabatini BL. et al. 2013. A nanobody-based system using fluorescent proteins as scaffolds for cell-specific gene manipulation. Cell 154:4928–39 [Google Scholar]
  99. Tervo DGR, Hwang B-Y, Viswanathan S, Gaj T, Lavzin M. et al. 2016. A designer AAV variant permits efficient retrograde access to projection neurons. Neuron 92:2372–82 [Google Scholar]
  100. Trapani I, Colella P, Sommella A, Iodice C, Cesi G. et al. 2014a. Effective delivery of large genes to the retina by dual AAV vectors. EMBO Mol. Med. 6:2194–211 [Google Scholar]
  101. Trapani I, Puppo A, Auricchio A. 2014b. Vector platforms for gene therapy of inherited retinopathies. Prog. Retin. Eye Res. 43:108–28 [Google Scholar]
  102. Tshilenge K-T, Baptiste A, Weber M, Mendes-Madeira A, Nedellec S. et al. 2016. Vitrectomy before intravitreal injection of AAV2/2 vector promotes efficient transduction of retinal ganglion cells in dogs and nonhuman primates. Hum. Gene Ther. Methods 27:3122–34 [Google Scholar]
  103. Vandenberghe LH, Bell P, Maguire AM, Cearley CN, Xiao R. et al. 2011. Dosage thresholds for AAV2 and AAV8 photoreceptor gene therapy in monkey. Sci. Transl. Med. 3:8888ra54 [Google Scholar]
  104. Vandenberghe LH, Bell P, Maguire AM, Xiao R, Hopkins TB. et al. 2013. AAV9 targets cone photoreceptors in the nonhuman primate retina. PLOS ONE 8:1e53463 [Google Scholar]
  105. Wang X. 2009. Cre transgenic mouse lines. Transgenesis Techniques: Principles and Protocols EJ Cartwright 265–73 Meth. Mol. Biol. 561 New York: Springer, 3rd ed.. [Google Scholar]
  106. Willett K, Bennett J. 2013. Immunology of AAV-mediated gene transfer in the eye. Front. Immunol. 4:261 [Google Scholar]
  107. Wojaczynski GJ, Engel EA, Steren KE, Enquist LW, Card JP. 2015. The neuroinvasive profiles of H129 (herpes simplex virus type 1) recombinants with putative anterograde-only transneuronal spread properties HHS public access. Brain Struct. Funct. 220:31395–420 [Google Scholar]
  108. Ye G-J, Budzynski E, Sonnentag P, Nork TM, Sheibani N. et al. 2016. Cone-specific promoters for gene therapy of achromatopsia and other retinal diseases. Hum. Gene Ther. 27:172–82 [Google Scholar]
  109. Yin L, Greenberg K, Hunter JJ, Dalkara D, Kolstad KD. et al. 2011. Intravitreal injection of AAV2 transduces macaque inner retina. Investig. Ophthalmol. Vis. Sci. 52:52775–83 [Google Scholar]
  110. Yonehara K, Farrow K, Ghanem A, Hillier D, Balint K. et al. 2013. The first stage of cardinal direction selectivity is localized to the dendrites of retinal ganglion cells. Neuron 79:61078–85 [Google Scholar]
  111. Zingg B, Chou X-l, Zhang Z-g, Mesik L, Liang F. et al. 2017. AAV-mediated anterograde transsynaptic tagging: mapping corticocollicular input-defined neural pathways for defense behaviors. Neuron 93:133–47 [Google Scholar]
  112. Zou J, Luo L, Shen Z, Chiodo VA, Ambati BK. et al. 2011. Whirlin replacement restores the formation of the USH2 protein complex in whirlin knockout photoreceptors. Investig. Opthalmol. Vis. Sci. 52:52343–51 [Google Scholar]
/content/journals/10.1146/annurev-vision-102016-061413
Loading
Vectors and Gene Delivery to the Retina
Annual Review of Vision Science 3, 121 (2017); https://doi.org/10.1146/annurev-vision-102016-061413
/content/journals/10.1146/annurev-vision-102016-061413
/content/journals/10.1146/annurev-vision-102016-061413
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