Clinical characteristics and current therapies for inherited retinal degenerations

Cold Spring Harbor Perspectives in Medicine

Volumn 5, Issue 2, 2015, Pages

  Sahel, José Alain ^{a,b,c,d,e,f,g}   Marazova, Katia ^a,b,c   Audo, Isabelle ^a,b,c,d,g  

^a SORBONNE UNIVERSITÉ   (France)

^b INSERM   (France)

^c CNRS   (France)

^d CENTRE HOSPITALIER NATIONAL D OPHTALMOLOGIE DES QUINZE VINGTS   (France)

^e FONDATION OPHTALMOLOGIQUE ADOLPHE DE ROTHSCHILD   (France)

^f Académie des Sciences Institut de France Paris   (France)

^g UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AGENTS ACTING ON THE EYE; MITOCHONDRIAL DNA;

ARTICLE; BARDET BIEDL SYNDROME; CELL TRANSPLANTATION; CHOROIDEREMIA; CLINICAL FEATURE; COLOR BLINDNESS; CONGENITAL STATIONARY NIGHT BLINDNESS; GENE THERAPY; HUMAN; INHERITED RETINA DEGENERATION; LEBER CONGENITAL AMAUROSIS; NEUROPROTECTION; NIGHT BLINDNESS; NONHUMAN; OPHTHALMOLOGICAL THERAPEUTIC DEVICE; OPTOGENETICS; PATHOPHYSIOLOGY; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); RETINA CELL; RETINA DEGENERATION; RETINA DYSTROPHY; RETINITIS PIGMENTOSA; RETINOSCHISIS; ROD CONE DYSTROPHY; SENSORY SUBSTITUTION DEVICE; SORSBY FUNDUS DYSTROPHY; STARGARDT DISEASE; USHER SYNDROME; VISUAL IMPAIRMENT; VITELLIFORM MACULAR DEGENERATION; X LINKED RETINOSCHISIS; ANIMAL; CLINICAL TRIAL (TOPIC); COLOR VISION DEFECT; DISEASE MODEL; EYE DISEASE; GENETIC HETEROGENEITY; GENETICS; MACULAR DEGENERATION; MYOPIA; PATHOLOGY; RETINAL DEGENERATION; X CHROMOSOME LINKED DISORDER;

ANIMALS; BARDET-BIEDL SYNDROME; CHOROIDEREMIA; CLINICAL TRIALS AS TOPIC; COLOR VISION DEFECTS; DISEASE MODELS, ANIMAL; EYE DISEASES, HEREDITARY; GENETIC DISEASES, X-LINKED; GENETIC HETEROGENEITY; GENETIC THERAPY; HUMANS; LEBER CONGENITAL AMAUROSIS; MACULAR DEGENERATION; MYOPIA; NIGHT BLINDNESS; OPTOGENETICS; RETINAL DEGENERATION;

EID: 84923815544     PISSN: None     EISSN: 21571422     Source Type: Journal    
DOI: 10.1101/cshperspect.a017111     Document Type: Article

References (180)

1. Acland GM, Aguirre GD, Ray J, Zhang Q, Aleman TS, Cideciyan AV, Pearce-Kelling SE, Anand V, Zeng Y, Maguire AM, et al. 2001. Gene therapy restores vision in a canine model of childhood blindness. Nat Genet 28: 92-95.
2. Acland GM, Aguirre GD, Bennett J, Aleman TS, Cideciyan AV, Bennicelli J, Dejneka NS, Pearce-Kelling SE, Maguire AM, Palczewski K, 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: 1072-1082.
3. Adackapara CA, Sunness JS, Dibernardo CW, Melia BM, Dagnelie G. 2008. Prevalence of cystoid macular edema and stability in oct retinal thickness in eyes with retinitis pigmentosa during a 48-week lutein trial. Retina 28: 103-110.
4. Aleman TS, Duncan JL, Bieber ML, de Castro E, Marks DA, Gardner LM, Steinberg JD, Cideciyan AV, Maguire MG, Jacobson SG. 2001. Macular pigment and lutein supple-mentation in retinitis pigmentosa and Usher syndrome. Invest Ophthalmol Vis Sci 42: 1873-1881.
5. Ali RR, Sarra GM, Stephens C, Alwis MD, Bainbridge JW, Munro PM, Fauser S, Reichel MB, Kinnon C, Hunt DM, et al. 2000. Restoration of photoreceptor ultrastructure and function in retinal degeneration slow mice by gene therapy. Nat Genet 25: 306-310.
6. Allikmets R, Singh N, Sun H, Shroyer NF, Hutchinson A, Chidambaram A, Gerrard B, Baird L, Stauffer D, Peiffer A, et al. 1997. A photoreceptor cell-specific ATP-binding transporter gene (ABCR) is mutated in recessive Star-gardt macular dystrophy. Nat Genet 15: 236-246.
7. Amado D, Mingozzi F, Hui D, Bennicelli JL, Wei Z, Chen Y, Bote E, Grant RL, Golden JA, Narfstrom K, et al. 2010. Safety and efficacy of subretinal readministration of a viral vector in large animals to treat congenital blindness. Sci Transl Med 2: 21ra16.
8. Andreasson SO, Sandberg MA, Berson EL. 1988. Narrow-band filtering for monitoring low-amplitude cone elec-troretinograms in retinitis pigmentosa. Am J Ophthalmol 105: 500-503.
9. Annear MJ, Bartoe JT, Barker SE, Smith AJ, Curran PG, Bainbridge JW, Ali RR, Petersen-Jones SM. 2011. Gene therapy in the second eye of RPE65-deficient dogs im-proves retinal function. Gene Ther 18: 53-61.
10. Audo I, Robson AG, Holder GE, Moore AT. 2008. The neg-ative ERG: Clinical phenotypes and disease mechanisms of inner retinal dysfunction. Surv Ophthalmol 53: 16-40.
11. Auricchio A, Kobinger G, Anand V, Hildinger M, O’Connor E, Maguire AM, Wilson JM, Bennett J. 2001. Exchange of surface proteins impacts on viral vector cellular specificity and transduction characteristics: The retina as a model. Hum Mol Genet 10: 3075-3081.
12. Auvray M, Hanneton S, O’Regan JK. 2007. Learning to perceive with a visuo-auditory substitution system: Localisation and object recognition with ‘the vOICe’. Perception 36: 416-430.
13. Ayuso C, Millan JM. 2010. Retinitis pigmentosa and allied conditions today: A paradigm of translational research. Genome Med 2: 34.
14. Bahrami H, Melia M, Dagnelie G. 2006. Lutein supplemen-tation in retinitis pigmentosa: PC-based vision assessment in a randomized double-masked placebo-controlled clinical trial [NCT00029289]. BMC Ophthalmol 6: 23.
15. Bainbridge JW, Smith AJ, Barker SS, Robbie S, Henderson R, Balaggan K, Viswanathan A, Holder GE, Stockman A, Tyler N, et al. 2008. Effect of gene therapy on visual function in Leber’s congenital amaurosis. N Engl J Med 358: 2231-2239.
16. Barker SE, Broderick CA, Robbie SJ, Duran Y, Natkunarajah M, Buch P, Balaggan KS, MacLaren RE, Bainbridge JW, Smith AJ, et al. 2009. Subretinal delivery of adeno-associated virus serotype 2 results in minimal immune responses that allow repeat vector administration in immunocompetent mice. J Gene Med 11: 486-497.
17. Bayyoud T, Bartz-Schmidt KU, Yoeruek E. 2013. Long-term clinical results after cataract surgery with and without capsular tension ring in patients with retinitis pigmentosa: A retrospective study. BMJ Open 26: e002616.
18. Bemelmans AP, Bonnel S, Houhou L, Dufour N, Nandrot E, Helmlinger D, Sarkis C, Abitbol M, Mallet J. 2005. Retinal cell type expression specificity of HIV-1-derived gene transfer vectors upon subretinal injection in the adult rat: Influence of pseudotyping and promoter. J Gene Med 7: 1367-1374.
19. Bennett J, Wilson J, Sun D, Forbes B, Maguire A. 1994. Adenovirus vector-mediated in vivo gene transfer into adult murine retina. Invest Ophthalmol Vis Sci 35: 2535-2542.
20. Bennett J, Tanabe T, Sun D, Zeng Y, Kjeldbye H, Gouras P, Maguire AM. 1996. Photoreceptor cell rescue in retinal degeneration (rd) mice by in vivo gene therapy. Nat Med 2: 649-654.
21. Bennett J, Ashtari M, Wellman J, Marshall KA, Cyckowski LL, Chung DC, McCague S, Pierce EA, Chen Y, Bennicelli JL, et al. 2012. AAV2 gene therapy readministration in three adults with congenital blindness. Sci Transl Med 4: 120ra115.
22. Bereta G, Kiser PD, Golczak M, Sun W, Heon E, Saperstein DA, Palczewski K. 2008. Impact of retinal disease-associated RPE65 mutations on retinoid isomerization. Biochemistry 47: 9856-9865.
23. Berson EL, Rosner B, Sandberg MA, Hayes KC, Nicholson BW, Weigel-DiFranco C, Willett W. 1993. A randomized trial of vitamin A and vitamin E supplementation for retinitis pigmentosa. Arch Ophthalmol 111: 761-772.
24. Berson EL, Rosner B, Sandberg MA, Weigel-DiFranco C, Moser A, Brockhurst RJ, Hayes KC, Johnson CA, Ander-son EJ, Gaudio AR, et al. 2004. Further evaluation of docosahexaenoic acid in patients with retinitis pigmentosa receiving vitamin A treatment: Subgroup analyses. Arch Ophthalmol 122: 1306-1314.
25. Berson EL, Rosner B, Sandberg MA, Weigel-DiFranco C, Brockhurst RJ, Hayes KC, Johnson EJ, Anderson EJ, John-son CA, Gaudio AR, et al. 2010. Clinical trial of lutein in patients with retinitis pigmentosa receiving vitamin A. Arch Ophthalmol 128: 403-411.
26. Bessant DA, Ali RR, Bhattacharya SS. 2001. Molecular genetics and prospects for therapy of the inherited retinal dystrophies. Curr Opin Genet Dev 11: 307-316.
27. Bhalla S, Joshi D, Bhullar S, Kasuga D, Park Y, Kay CN. 2013. Long-term follow-up for efficacy and safety of treatment of retinitis pigmentosa with valproic acid. Br J Ophthalmol 97: 895-899.
28. Birch DG, Sandberg MA. 1996. Submicrovolt full-field cone electroretinograms: Artifacts and reproducibility. Doc Ophthalmol 92: 269-280.
29. Birch DG., Weleber RG, Duncan JL, Jaffe GJ., Tao W. 2013. Randomized trial of ciliary neurotrophic factor delivered by encapsulated cell intraocular implants for retinitis pigmentosa. Am J Ophthalmol 156: 283-292.
30. Blacharski P. 1988. Fundus flavimaculatus. In Retinal dystrophies and degenerations (ed. Newsome DA), pp. 135-159. Raven, New York.
31. Boughman JA, Vernon M, Shaver KA. 1983. Usher syndrome: Definition and estimate of prevalence from two high-risk populations. J Chronic Dis 36: 595-603.
32. Boyden ES, Zhang F, Bamberg E, Nagel G, Deisseroth K. 2005. Millisecond-timescale, genetically targeted optical control of neural activity. Nat Neurosci 8: 1263-1268.
33. Bunker CH, Berson EL, Bromley WC, Hayes RP, Roderick TH. 1984. Prevalence of retinitis pigmentosa in Maine. Am J Ophthalmol 97: 357-365.
34. Busskamp V, Duebel J, Balya D, Fradot M, Viney TJ, Siegert S, Groner AC, Cabuy E, Forster V, Seeliger M, et al. 2010. Genetic reactivation of cone photoreceptors restores visual responses in retinitis pigmentosa. Science 329: 413-417.
35. Busskamp V, Picaud S, Sahel JA, Roska B. 2011. Optogenetic therapy for retinitis pigmentosa. Gene Ther 19: 169-175.
36. Chebat DR, Rainville C, Kupers R, Ptito M. 2007. Tactile-‘visual’ acuity of the tongue in early blind individuals. Neuroreport 18: 1901-1904.
37. Cideciyan AV, Aleman TS, Swider M, Schwartz SB, Steinberg JD, Brucker AJ, Maguire AM, Bennett J, Stone EM, Ja-cobson SG. 2004. Mutations in ABCA4 result in accumulation of lipofuscin before slowing of the retinoid cycle: A reappraisal of the human disease sequence. Hum Mol Genet 13: 525-534.
38. Cideciyan AV, Jacobson SG, Beltran WA, Sumaroka A, Swider M, Iwabe S, Roman AJ, Olivares MB, Schwartz SB, Komaromy AM, et al. 2013. Human retinal gene therapy for Leber congenital amaurosis shows advancing retinal degeneration despite enduring visual improvement. Proc Natl Acad Sci 110: E517-E525.
39. Clemson CM, Tzekov R, Krebs M, Checchi JM, Bigelow C, Kaushal S. 2011. Therapeutic potential of valproic acid for retinitis pigmentosa. Br J Ophthalmol 95: 89-93.
40. Colella P, Auricchio A. 2010. AAV-mediated gene supply for treatment of degenerative and neovascular retinal diseases. Curr Gene Ther 10: 371-380.
41. Conlon TJ, Deng WT, Erger K, Cossette T, Pang JJ, Ryals R, Clement N, Cleaver B, McDoom I, Boye SE, 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: 23-28.
42. Coppieters F, Lefever S, Leroy BP, De Baere E. 2010. CEP290, a gene with many faces: Mutation overview and presentation of CEP290base. Hum Mutat 31: 1097-1108.
43. Cramer AO, MacLaren RE. 2013. Translating induced pluripotent stem cells from bench to bedside: Application to retinal diseases. Curr Gene Ther 13: 139-151.
44. Cremers FP, van de Pol DJ, van Kerkhoff LP, Wieringa B, Ropers HH. 1990. Cloning of a gene that is rearranged in patients with choroideraemia. Nature 347: 674-677.
45. Cremers FP, van de Pol DJ, van Driel M, den Hollander AI, van Haren FJ, Knoers NV, Tijmes N, Bergen AA, Rohrsch-neider K, Blankenagel A, et al. 1998. Autosomal recessive retinitis pigmentosa and cone-rod dystrophy caused by splice site mutations in the Stargardt’s disease gene ABCR. Hum Mol Genet 7: 355-362.
46. da Cruz L, Coley BF, Dorn J, Merlini F, Filley E, Christopher P, Chen FK, Wuyyuru V, Sahel J, Stanga P, et al. 2013. The Argus II epiretinal prosthesis system allows letter and word reading and long-term function in patients with profound vision loss. Br J Ophthalmol 97: 632-636.
47. Daiger SP, Bowne SJ, Sullivan LS. 2007. Perspective on genes and mutations causing retinitis pigmentosa. Arch Oph-thalmol 125: 151-158.
48. Dalkara D, Byrne LC, Klimczak RR, Visel M, Yin L, Merigan WH, Flannery JG, Schaffer DV. 2013. In vivo-directed evolution of a new adeno-associated virus for therapeutic outer retinal gene delivery from the vitreous. Sci Transl Med 5: p 189ra176.
49. den Hollander AI, Roepman R, Koenekoop RK, Cremers FP. 2008. Leber congenital amaurosis: Genes, proteins and disease mechanisms. Prog Retin Eye Res 27: 391-419.
50. Dikopf MS, Chow CC, Mieler WF, Tu EY. 2013. Cataract extraction outcomes and the prevalence of zonular insufficiency in retinitis pigmentosa. Am J Ophthalmol 156: 82-88.
51. Drivas TG, Holzbaur EL, Bennett J. 2013. Disruption of CEP290 microtubule/membrane-binding domains causes retinal degeneration. J Clin Invest 123: 4525-4539.
52. Dryja TP. 2000. Molecular genetics of Oguchi disease, fundus albipunctatus, and other forms of stationary night blindness: LVII Edward Jackson Memorial Lecture. Am J Ophthalmol 130: 547-563.
53. Dryja TP, McGee TL, Reichel E, Hahn LB, Cowley GS, Yan-dell DW, Sandberg MA, Berson EL. 1990. A point mutation of the rhodopsin gene in one form of retinitis pigmentosa. Nature 343: 364-366.
54. Dryja TP, Finn JT, Peng YW, McGee TL, Berson EL, Yau KW. 1995. Mutations in the gene encoding the a subunit of the rod cGMP-gated channel in autosomal recessive retinitis pigmentosa. Proc Natl Acad Sci 92: 10177-10181.
55. Falk MJ, Zhang Q, Nakamaru-Ogiso E, Kannabiran C, Fon-seca-Kelly Z, Chakarova C, Audo I, Mackay DS, Zeitz C, Borman AD, et al. 2012. NMNAT1 mutations cause Leber congenital amaurosis. Nat Genet 44: 1040-1045.
56. Farkas MH, Grant GR, White JA, Sousa ME, Consugar MB, Pierce EA. 2013. Transcriptome analyses of the human retina identify unprecedented transcript diversity and 3.5 Mb of novel transcribed sequence via significant alternative splicing and novel genes. BMC Genomics 14: 486.
57. Farrar GJ, Palfi A, O’Reilly M. 2010. Gene therapeutic approaches for dominant retinopathies. Curr Gene Ther 10: 381-388.
58. Fishman GA, Anderson RJ, Lourenco P. 1985. Prevalence of posterior subcapsular lens opacities in patients with retinitis pigmentosa. Br J Ophthalmol 69: 263-266.
59. Fishman GA, Gilbert LD, Fiscella RG, Kimura AE, Jampol LM. 1989. Acetazolamide for treatment of chronic macular edema in retinitis pigmentosa. Arch Ophthalmol 107: 1445-1452.
60. Forsythe E, Beales PL. 2012. Bardet-Biedl syndrome. Eur J Hum Genet 21: 8-13.
61. Frasson M, Sahel JA, Fabre M, Simonutti M, Dreyfus H, Picaud S. 1999. Retinitis pigmentosa: Rod photoreceptor rescue by a calcium-channel blocker in the rd mouse. Nat Med 5: 1183-1187.
62. Genead MA, Fishman GA, Rha J, Dubis AM, Bonci DM, Dubra A, Stone EM, Neitz M, Carroll J. 2011. Photoreceptor structure and function in patients with congenital achromatopsia. Invest Ophthalmol Vis Sci 52: 7298-7308.
63. George ND, Yates JR, Moore AT. 1995. X linked retinoschisis. Br J Ophthalmol 79: 697-702.
64. George ND, Yates JR, Moore AT. 1996. Clinical features in affected males with X-linked retinoschisis. Arch Ophthal-mol 114: 274-280.
65. Gerber S, Rozet JM, Bonneau D, Souied E, Camuzat A, Dufier JL, Amalric P, Weissenbach J, Munnich A, Kaplan J. 1995. A gene for late-onset fundus flavimaculatus with macular dystrophy maps to chromosome 1p13. Am J Hum Genet 56: 396-399.
66. Gocho K, Sarda V, Falah S, Sahel JA, Sennlaub F, Bencha-boune M, Ullern M, Paques M. 2013. Adaptive optics imaging of geographic atrophy. Invest Ophthalmol Vis Sci 54: 3673-3680.
67. Goldberg NR, Greenberg JP, Laud K, Tsang S, Freund KB. 2013. Outer retinal tubulation in degenerative retinal disorders. Retina 33: 1871-1876.
68. Gonzalez-Cordero A, West EL, Pearson RA, Duran Y, Car-valho LS, Chu CJ, Naeem A, Blackford SJ, Georgiadis A, Lakowski J, et al. 2013. Photoreceptor precursors derived from three-dimensional embryonic stem cell cultures integrate and mature within adult degenerate retina. Nat Biotechnol 31: 741-747.
69. Grover S, Fishman GA, Fiscella RG, Adelman AE. 1997. Efficacy of dorzolamide hydrochloride in the management of chronic cystoid macular edema in patients with retinitis pigmentosa. Retina 17: 222-231.
70. Hagiwara A, Yamamoto S, Ogata K, Sugawara T, Hiramatsu A, Shibata M, Mitamura Y. 2011. Macular abnormalities in patients with retinitis pigmentosa: Prevalence on OCT examination and outcomes of vitreoretinal surgery. Acta Ophthalmol 89: e122-e125.
71. Haim M. 2002. Epidemiology of retinitis pigmentosa in Denmark. Acta Ophthalmol Scand 80(S233): 1-34.
72. Hartong DT, Berson EL, Dryja TP. 2006. Retinitis pigmen-tosa. Lancet 368: 1795-1809.
73. Hauswirth WW, Aleman TS, Kaushal S, Cideciyan AV, Schwartz SB, Wang L, Conlon TJ, Boye SL, Flotte TR, Byrne BJ, 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: 979-990.
74. Heckenlively J. 1982. The frequency of posterior subcapsular cataract in the hereditary retinal degenerations. Am J Ophthalmol 93: 733-738.
75. Heckenlively JR, Yoser SL, Friedman LH, Oversier JJ. 1988. Clinical findings and common symptoms in retinitis pigmentosa. Am J Ophthalmol 105: 504-511.
76. Hirami Y, Osakada F, Takahashi K, Okita K, Yamanaka S, Ikeda H, Yoshimura N, Takahashi M. 2009. Generation of retinal cells from mouse and human induced pluripotent stem cells. Neurosci Lett 458: 126-131.
77. Hoffman LM, Maguire AM, Bennett J. 1997. Cell-mediated immune response and stability of intraocular transgene expression after adenovirus-mediated delivery. Invest Ophthalmol Vis Sci 38: 2224-2233.
78. Hoffman DR, Locke KG, Wheaton DH, Fish GE, Spencer R, Birch DG. 2004. A randomized, placebo-controlled clinical trial of docosahexaenoic acid supplementation for X-linked retinitis pigmentosa. Am J Ophthalmol 137: 704-718.
79. Hood DC, Holopigian K, Greenstein V, Seiple W, Li J, Sutter EE, Carr RE. 1998. Assessment of local retinal function in patients with retinitis pigmentosa using the multi-focal ERG technique. Vision Res 38: 163-179.
80. Humayun MS, de Juan E Jr, Dagnelie G, Greenberg RJ, Propst RH, Phillips DH. 1996. Visual perception elicited by electrical stimulation of retina in blind humans. Arch Ophthalmol 114: 40-46.
81. Humayun MS, Weiland JD, Fujii GY, Greenberg R, William-son R, Little J, Mech B, Cimmarusti V, Van Boemel G, Dagnelie G, et al. 2003. Visual perception in a blind subject with a chronic microelectronic retinal prosthesis. Vision Res 43: 2573-2581.
82. Humayun MS, Dorn JD, da Cruz L, Dagnelie G, Sahel JA, Stanga PE, Cideciyan AV, Duncan JL, Eliott D, Filley E, et al. 2012. Interim results from the international trial of Second Sight’s visual prosthesis. Ophthalmology 119: 779-788.
83. Jackson H, Garway-Heath D, Rosen P, Bird AC, Tuft SJ. 2001. Outcome of cataract surgery in patients with retinitis pigmentosa. Br J Ophthalmol 85: 936-938.
84. Jacobson SG, Cideciyan AV, Ratnakaram R, Heon E, Schwartz SB, Roman AJ, Peden MC, Aleman TS, Boye SL, Sumaroka A, et al. 2012. Gene therapy for Leber congenital amaurosis caused by RPE65 mutations: Safety and efficacy in 15 children and adults followed up to 3 years. Arch Ophthalmol 130: 9-24.
85. Janssen A, Min SH, Molday LL, Tanimoto N, Seeliger MW, Hauswirth WW, Molday RS, Weber BH. 2008. Effect of late-stage therapy on disease progression in AAV-mediated rescue of photoreceptor cells in the retinoschisin-deficient mouse. Mol Ther 16: 1010-1017.
86. Jonas JB, Xu L, Wang YX. 2009. The Beijing Eye Study. Acta Ophthalmol 87: 247-261.
87. Kamenarova K, Cherninkova S, Romero Duran M, Prescott D, Valdes Sanchez ML, Mitev V, Kremensky I, Kaneva R, Bhattacharya SS, Tournev I, et al. 2013. A novel locus for autosomal dominant cone-rod dystrophy maps to chromosome 10q. Eur J Hum Genet 21: 338-342.
88. Kauper K, McGovern C, Sherman S, Heatherton P, Rapoza R, Stabila P, Dean B, Lee A, Borges S, Bouchard B, et al. 2012. Two-year intraocular delivery of ciliary neurotrophic factor by encapsulated cell technology implants in patients with chronic retinal degenerative diseases. Invest Ophthalmol Vis Sci 53: 7484-7491.
89. Kjellstrom S, Bush RA, Zeng Y, Takada Y, Sieving PA. 2007. Retinoschisin gene therapy and natural history in the Rs1h-KO mouse: Long-term rescue from retinal degeneration. Invest Ophthalmol Vis Sci 48: 3837-3845.
90. Koenekoop RK. 2004. An overview of Leber congenital amaurosis: A model to understand human retinal development. Surv Ophthalmol 49: 379-398.
91. Koenekoop RK, Wang H, Majewski J, Wang X, Lopez I, Ren H, Chen Y, Li Y, Fishman GA, Genead M, et al. 2012. Mutations in NMNAT1 cause Leber congenital amaurosis and identify a new disease pathway for retinal degeneration. Nat Genet 44: 1035-1039.
92. Kohl S, Hamel C. 2013. Clinical utility gene card for: Achromatopsia-update 2013. Eur J Hum Genet 21. http://www.nature.com/ejhg/journal/v21/n11/full/ejhg201344a.html
93. Kohl S, Coppieters F, Meire F, Schaich S, Roosing S, Bren-nenstuhl C, Bolz S, van Genderen MM, Riemslag FC, Lukowski R, et al. 2012. A nonsense mutation in PDE6H causes autosomal-recessive incomplete achro-matopsia. Am J Hum Genet 91: 527-532.
94. Koizumi H, Spaide RF, Fisher YL, Freund KB, Klancnik JM Jr, Yannuzzi LA. 2008. Three-dimensional evaluation of vitreomacular traction and epiretinal membrane using spectral-domain optical coherence tomography. Am J Ophthalmol 145: 509-517.
95. Komaromy AM, Alexander JJ, Rowlan JS, Garcia MM, Chiodo VA, Kaya A, Tanaka JC, Acland GM, Hauswirth WW, Aguirre GD. 2010. Gene therapy rescues cone function in congenital achromatopsia. Hum Mol Genet 19: 2581-2593.
96. Kong J, Kim SR, Binley K, Pata I, Doi K, Mannik J, Zernant-Rajang J, Kan O, Iqball S, Naylor S, et al. 2008. Correction of the disease phenotype in the mouse model of Stargardt disease by lentiviral gene therapy. Gene Ther 15: 1311-1320.
97. Lagali PS, Balya D, Awatramani GB, Munch TA, Kim DS, Busskamp V, Cepko CL, Roska B. 2008. Light-activated channels targeted to ON bipolar cells restore visual function in retinal degeneration. Nat Neurosci 11: 667-675.
98. Lamba DA, Gust J, Reh TA. 2009. Transplantation of human embryonic stem cell-derived photoreceptors restores some visual function in Crx-deficient mice. Cell Stem Cell 4: 73-79.
99. Lamba DA, McUsic A, Hirata RK, Wang PR, Russell D, Reh TA. 2010. Generation, purification and transplantation of photoreceptors derived from human induced pluripotent stem cells. PLoS ONE 5: e8763.
100. Lauritzen TZ, Harris J, Mohand-Said S, Sahel JA, Dorn JD, McClure K, Greenberg RJ. 2012. Reading visual Braille with a retinal prosthesis. Front Neurosci 6: 168.
101. Leveillard T, Sahel JA. 2010. Rod-derived cone viability factor for treating blinding diseases: From clinic to redox signaling. Sci Transl Med 2: 26ps16.
102. Leveillard T, Mohand-Said S, Lorentz O, Hicks D, Fintz AC, Clerin E, Simonutti M, Forster V, Cavusoglu N, Chalmel F, et al. 2004. Identification and characterization of rod-derived cone viability factor. Nat Genet 36: 755-759.
103. Li ZY, Kljavin IJ, Milam AH. 1995. Rod photoreceptor neurite sprouting in retinitis pigmentosa. J Neurosci 15: 5429-5438.
104. Lin B, Masland RH, Strettoi E. 2009. Remodeling of cone photoreceptor cells after rod degeneration in rd mice. Exp Eye Res 88: 589-599.
105. Liu X, Ondek B, Williams DS. 1998. Mutant myosin VIIa causes defective melanosome distribution in the RPE of shaker-1 mice. Nat Genet 19: 117-118.
106. Liu X, Udovichenko IP, Brown SD, Steel KP, Williams DS. 1999. Myosin VIIa participates in opsin transport through the photoreceptor cilium. J Neurosci 19: 6267-6274.
107. Lois N, Holder GE, Bunce C, Fitzke FW, Bird AC. 2001. Phenotypic subtypes of Stargardt macular dystrophy-fundus flavimaculatus. Arch Ophthalmol 119: 359-369.
108. MacLaren RE, Pearson RA, MacNeil A, Douglas RH, Salt TE, Akimoto M, Swaroop A, Sowden JC, Ali RR. 2006. Retinal repair by transplantation of photoreceptor precursors. Nature 444: 203-207.
109. MacLaren RE, Groppe M, Barnard AR, Cottriall CL, Tolma-chova T, Seymour L, Clark KR, During MJ, Cremers FP, Black GC, et al. 2014. Retinal gene therapy in patients with choroideremia: Initial findings from a phase 1/2 clinical trial. Lancet 383: 1129-1137.
110. Maeda T, Cideciyan AV, Maeda A, Golczak M, Aleman TS, Jacobson SG, Palczewski K. 2009. Loss of cone photore-ceptors caused by chromophore depletion is partially prevented by the artificial chromophore pro-drug, 9-cis-retinyl acetate. Hum Mol Genet 18: 2277-2287.
111. Maeda T, Dong Z, Jin H, Sawada O, Gao S, Utkhede D, Monk W, Palczewska G, Palczewski K. 2013. QLT091001, a 9-cis-retinal analog, is well-tolerated by retinas of mice with impaired visual cycles. Invest Oph-thalmol Vis Sci 54: 455-466.
112. Maguire AM, Simonelli F, Pierce EA, Pugh EN Jr, Mingozzi F, Bennicelli J, Banfi S, Marshall KA, Testa F, Surace EM, et al. 2008. Safety and efficacy of gene transfer for Leber’s congenital amaurosis. N Engl J Med 358: 2240-2248.
113. Mathieson K, Loudin J, Goetz G, Huie P, Wang L, Kamins TI, Galambos L, Smith R, Harris JS, Sher A, et al. 2012. Photovoltaic retinal prosthesis with high pixel density. Nat Photonics 6: 391-397.
114. McLaughlin ME, Sandberg MA, Berson EL, Dryja TP. 1993. Recessive mutations in the gene encoding the b-subunit of rod phosphodiesterase in patients with retinitis pig-mentosa. Nat Genet 4: 130-134.
115. Merabet LB, Battelli L, Obretenova S, Maguire S, Meijer P, Pascual-Leone A. 2009. Functional recruitment of visual cortex for sound encoded object identification in the blind. Neuroreport 20: 132-138.
116. Michaelides M, Hunt DM, Moore AT. 2004. The cone dys-function syndromes. Br J Ophthalmol 88: 291-297.
117. Mitamura Y, Mitamura-Aizawa S, Nagasawa T, Katome T, Eguchi H, Naito T. 2012. Diagnostic imaging in patients with retinitis pigmentosa. J Med Invest 59: 1-11.
118. Miyake Y, Yagasaki K, Horiguchi M, Kawase Y, Kanda T. 1986. Congenital stationary night blindness with negative electroretinogram. A new classification. Arch Ophthalmol 104: 1013-1020.
119. Murakami T, Akimoto M, Ooto S, Suzuki T, Ikeda H, Ka-wagoe N, Takahashi M, Yoshimura N. 2008. Association between abnormal autofluorescence and photoreceptor disorganization in retinitis pigmentosa. Am J Ophthalmol 145: 687-694.
120. Nagel G, Ollig D, Fuhrmann M, Kateriya S, Musti AM, Bamberg E, Hegemann P. 2002. Channelrhodopsin-1: A light-gated proton channel in green algae. Science 296: 2395-2398.
121. Nakazawa M, Ohguro H, Takeuchi K, Miyagawa Y, Ito T, Metoki T. 2011. Effect of nilvadipine on central visual field in retinitis pigmentosa: A 30-month clinical trial. Ophthalmologica 225: 120-126.
122. Naldini L, Blomer U, Gallay P, Ory D, Mulligan R, Gage FH, Verma IM, Trono D. 1996. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272: 263-267.
123. Nangia V, Jonas JB, Khare A, Sinha A. 2012. Prevalence of retinitis pigmentosa in India: The Central India Eye and Medical Study. Acta Ophthalmol 90: e649-e650.
124. Novarino G, Akizu N, Gleeson JG. 2011. Modeling human disease in humans: The ciliopathies. Cell 147: 70-79.
125. Osakada F, Ikeda H, Mandai M, Wataya T, Watanabe K, Yoshimura N, Akaike A, Sasai Y, Takahashi M. 2008. To-ward the generation of rod and cone photoreceptors from mouse, monkey and human embryonic stem cells. Nat Biotechnol 26: 215-224.
126. Park TK, Wu Z, Kjellstrom S, Zeng Y, Bush RA, Sieving PA, Colosi P. 2009. Intravitreal delivery of AAV8 retinoschisin results in cell type-specific gene expression and retinal rescue in the Rs1-KO mouse. Gene Ther 16: 916-926.
127. Petit C. 2001. Usher syndrome: From genetics to pathogenesis. Annu Rev Genomics Hum Genet 2: 271-297.
128. Pimenides D, George ND, Yates JR, Bradshaw K, Roberts SA, Moore AT, Trump D. 2005. X-linked retinoschisis: Clinical phenotype and RS1 genotype in 86 UK patients. J Med Genet 42: e35.
129. Potter MJ, Wong E, Szabo SM, McTaggart KE. 2004. Clinical findings in a carrier of a new mutation in the choroideremia gene. Ophthalmology 111: 1905-1909.
130. Preising M, Ayuso C. 2004. Rab escort protein 1 (REP1) in intracellular traffic: A functional and pathophysiological overview. Ophthalmic Genet 25: 101-110.
131. Prokisch H, Hartig M, Hellinger R, Meitinger T, Rosenberg T. 2007. A population-based epidemiological and genetic study of X-linked retinitis pigmentosa. Invest Ophthalmol Vis Sci 48: 4012-4018.
132. Radtke ND, Aramant RB, Petry HM, Green PT, Pidwell DJ, Seiler MJ. 2008. Vision improvement in retinal de-generation patients by implantation of retina together with retinal pigment epithelium. Am J Ophthalmol 146: 172-182.
133. Renner AB, Kellner U, Cropp E, Preising MN, MacDonald IM, van den Hurk JA, Cremers FP, Foerster MH. 2006. Choroideremia: Variability of clinical and electrophysio-logical characteristics and first report of a negative elec-troretinogram. Ophthalmology 113: 2066.e1-e10.
134. The Retinoschisis Consortium. 1998. Functional implica-tions of the spectrum of mutations found in 234 cases with X-linked juvenile retinoschisis (XLRS). Hum Mol Genet 7: 1185-1192.
135. Robson AG, El-Amir A, Bailey C, Egan CA, Fitzke FW, Web-ster AR, Bird AC, Holder GE. 2003. Pattern ERG corre-lates of abnormal fundus autofluorescence in patients with retinitis pigmentosa and normal visual acuity. Invest Ophthalmol Vis Sci 44: 3544-3550.
136. Robson AG, Tufail A, Fitzke F, Bird AC, Moore AT, Holder GE, Webster AR. 2011. Serial imaging and structure-function correlates of high-density rings of fundus au-tofluorescence in retinitis pigmentosa. Retina 31: 1670-1679.
137. Roepman R, van Duijnhoven G, Rosenberg T, Pinckers AJ, Bleeker-Wagemakers LM, Bergen AA, Post J, Beck A, Reinhardt R, Ropers HH, et al. 1996. Positional cloning of the gene for X-linked retinitis pigmentosa 3: Homol-ogy with the guanine-nucleotide-exchange factor RCC1. Hum Mol Genet 5: 1035-1041.
138. Romani M, Micalizzi A, Valente EM. 2013. Joubert syndrome: Congenital cerebellar ataxia with the molar tooth. Lancet Neurol 12: 894-905.
139. Ronquillo CC, Bernstein PS, Baehr W. 2012. Senior-Loken syndrome: A syndromic form of retinal dystrophy associated with nephronophthisis. Vision Res 75: 88-97.
140. Rosenfeld PJ, Cowley GS, McGee TL, Sandberg MA, Berson EL, Dryja TP. 1992. A null mutation in the rhodopsin gene causes rod photoreceptor dysfunction and autosomal recessive retinitis pigmentosa. Nat Genet 1: 209-213.
141. Sahel JA, Roska B. 2013. Gene therapy for blindness. Annu Rev Neurosci 36: 467-488.
142. Sampaio E, Maris S, Bach-y-Rita P. 2001. Brain plasticity: ‘Visual’ acuity of blind persons via the tongue. Brain Res 908: 204-207.
143. Sauer CG, Gehrig A, Warneke-Wittstock R, Marquardt A, Ewing CC, Gibson A, Lorenz B, Jurklies B, Weber BH. 1997. Positional cloning of the gene associated with X-linked juvenile retinoschisis. Nat Genet 17: 164-170.
144. Schwartz SD, Hubschman JP, Heilwell G, Franco-Cardenas V, Pan CK, Ostrick RM, Mickunas E, Gay R, Klimanskaya I, Lanza R. 2012. Embryonic stem cell trials for macular degeneration: A preliminary report. Lancet 379: 713-720.
145. Sen P, Bhargava A, George R, Ve Ramesh S, Hemamalini A, Prema R, Kumaramanickavel G, Vijaya L. 2008. Preva-lence of retinitis pigmentosa in South Indian population aged above 40 years. Ophthalmic Epidemiol 15: 279-281.
146. Sidjanin DJ, Lowe JK, McElwee JL, Milne BS, Phippen TM, Sargan DR, Aguirre GD, Acland GM, Ostrander EA. 2002. Canine CNGB3 mutations establish cone degeneration as orthologous to the human achromatopsia locus ACHM3. Hum Mol Genet 11: 1823-1833.
147. Sieving PA, Arnold EB, Jamison J, Liepa A, Coats C. 1998. Submicrovolt flicker electroretinogram: Cycle-by-cycle recording of multiple harmonics with statistical estimation of measurement uncertainty. Invest Ophthalmol Vis Sci 39: 1462-1469.
148. Sieving PA, Bingham EL, Kemp J, Richards J, Hiriyanna K. 1999. Juvenile X-linked retinoschisis from XLRS1 Arg213Trp mutation with preservation of the electroret-inogram scotopic b-wave. Am J Ophthalmol 128: 179-184.
149. Sieving PA, Caruso RC, Tao W, Coleman HR, Thompson DJ, Fullmer KR, Bush RA. 2006. Ciliary neurotrophic factor (CNTF) for human retinal degeneration: Phase I trial of CNTF delivered by encapsulated cell intraocular implants. Proc Natl Acad Sci 103: 3896-3901.
150. Stargardt K. 1909. Uber familiäre, progressive degeneration under makulagegend des auges. Albrecht von Graefes Arch Ophthalmol 71: 534-550.
151. Stingl K, Bartz-Schmidt KU, Besch D, Braun A, Bruckmann A, Gekeler F, Greppmaier U, Hipp S, Hortdorfer G, Kern-stock C, et al. 2013. Artificial vision with wirelessly powered subretinal electronic implant a-IMS. Proc Biol Sci 280: 20130077.
152. Striem-Amit E, Dakwar O, Reich L, Amedi A. 2011. The large-scale organization of “visual” streams emerges without visual experience. Cereb Cortex 22: 1698-1709.
153. Striem-Amit E, Cohen L, Dehaene S, Amedi A. 2012a. Reading with sounds: Sensory substitution selectively activates the visual word form area in the blind. Neuron 76: 640-652.
154. Striem-Amit E, Guendelman M, Amedi A. 2012b. ‘Visual’ acuity of the congenitally blind using visual-to-auditory sensory substitution. PLoS ONE 7: e33136.
155. Sun H, Nathans J. 1997. Stargardt’s ABCR is localized to the disc membrane of retinal rod outer segments. Nat Genet 17: 15-16.
156. Takano Y, Ohguro H, Dezawa M, Ishikawa H, Yamazaki H, Ohguro I, Mamiya K, Metoki T, Ishikawa F, Nakazawa M. 2004. Study of drug effects of calcium channel blockers on retinal degeneration of rd mouse. Biochem Biophys Res Commun 313: 1015-1022.
157. Talcott KE, Ratnam K, Sundquist SM, Lucero AS, Lujan BJ, Tao W, Porco TC, Roorda A, Duncan JL. 2011. Longitu-dinal study of cone photoreceptors during retinal degen-eration and in response to ciliary neurotrophic factor treatment. Invest Ophthalmol Vis Sci 52: 2219-2226.
158. Testa F, Maguire AM, Rossi S, Pierce EA, Melillo P, Marshall K, Banfi S, Surace EM, Sun J, Acerra C, et al. 2013. Three-year follow-up after unilateral subretinal delivery of adeno-associated virus in patients with Leber congenital amaurosis type 2. Ophthalmology 120: 1283-1291.
159. Thompson DA, Li Y, McHenry CL, Carlson TJ, Ding X, Sieving PA, Apfelstedt-Sylla E, Gal A. 2001. Mutations in the gene encoding lecithin retinol acyltransferase are associated with early-onset severe retinal dystrophy. Nat Genet 28: 123-124.
160. Tojo N, Nakamura T, Fuchizawa C, Oiwake T, Hayashi A. 2013. Adaptive optics fundus images of cone photorecep-tors in the macula of patients with retinitis pigmentosa. Clin Ophthalmol 7: 203-210.
161. Tolmachova T, Tolmachov OE, Wavre-Shapton ST, Tracey-White D, Futter CE, Seabra MC. 2012. CHM/REP1 cDNA delivery by lentiviral vectors provides functional expression of the transgene in the retinal pigment epithet-lium of choroideremia mice. J Gene Med 14: 158-168.
162. Tschernutter M, Schlichtenbrede FC, Howe S, Balaggan KS, Munro PM, Bainbridge JW, Thrasher AJ, Smith AJ, Ali RR. 2005. Long-term preservation of retinal function in the RCS rat model of retinitis pigmentosa following len-tivirus-mediated gene therapy. Gene Ther 12: 694-701.
163. Tsujikawa M, Wada Y, Sukegawa M, Sawa M, Gomi F, Nish-ida K, Tano Y. 2008. Age at onset curves of retinitis pig-mentosa. Arch Ophthalmol 126: 337-340.
164. Tsybovsky Y, Molday RS, Palczewski K. 2010. The ATP-bind-ing cassette transporter ABCA4: Structural and functional properties and role in retinal disease. Adv Exp Med Biol 703: 105-125.
165. Van Hooser JP, Aleman TS, He YG, Cideciyan AV, Kuksa V, Pittler SJ, Stone EM, Jacobson SG, Palczewski K. 2000. Rapid restoration of visual pigment and function with oral retinoid in a mouse model of childhood blindness. Proc Natl Acad Sci 97: 8623-8628.
166. van Reeuwijk J, Arts HH, Roepman R. 2011. Scrutinizing ciliopathies by unraveling ciliary interaction networks. Hum Mol Genet 20: R149-R157.
167. Vandenberghe LH, Auricchio A. 2012. Novel adeno-associated viral vectors for retinal gene therapy. Gene Ther 19: 162-168.
168. Vasireddy V, Mills JA, Gaddameedi R, Basner-Tschakarjan E, Kohnke M, Black AD, Alexandrov K, Zhou S, Maguire AM, Chung DC, et al. 2013. AAV-mediated gene therapy for Choroideremia: Preclinical studies in personalized models. PLoS ONE 8: e61396.
169. Waters AM, Beales PL. 2011. Ciliopathies: An expanding disease spectrum. Pediatr Nephrol 26: 1039-1056.
170. Witkin AJ, Ko TH, Fujimoto JG, Chan A, Drexler W, Schu-man JS, Reichel E, Duker JS. 2006. Ultra-high resolution optical coherence tomography assessment of photore-ceptors in retinitis pigmentosa and related diseases. Am J Ophthalmol 142: 945-952.
171. Yang Y, Mohand-Said S, Danan A, Simonutti M, Fontaine V, Clerin E, Picaud S, Leveillard T, Sahel JA. 2009. Function-al cone rescue by RdCVF protein in a dominant model of retinitis pigmentosa. Mol Ther 17: 787-795.
172. Yatsenko AN, Shroyer NF, Lewis RA, Lupski JR. 2001. Late-onset Stargardt disease is associated with missense mutations that map outside known functional regions of ABCR (ABCA4). Hum Genet 108: 346-355.
173. You QS, Xu L, Wang YX, Liang QF, Cui TT, Yang XH, Wang S, Yang H, Jonas JB. 2013. Prevalence of retinitis pigmen-tosa in North China: The Beijing Eye Public Health Care Project. Acta Ophthalmol 91: e499-e500.
174. Zeitz C, Jacobson SG, Hamel CP, Bujakowska K, Neuille M, Orhan E, Zanlonghi X, Lancelot ME, Michiels C, Schwartz SB, et al. 2013. Whole-exome sequencing identifies LRIT3 mutations as a cause of autosomal-recessive complete congenital stationary night blindness. Am J Hum Genet 92: 67-75.
175. Zeng Y, Takada Y, Kjellstrom S, Hiriyanna K, Tanikawa A, Wawrousek E, Smaoui N, Caruso R, Bush RA, Sieving PA. 2004. RS-1 gene delivery to an adult Rs1h knockout mouse model restores ERG b-wave with reversal of the electronegative waveform of X-linked retinoschisis. Invest Ophthalmol Vis Sci 45: 3279-3285.
176. Zhang K, Kniazeva M, Han M, Li W, Yu Z, Yang Z, Li Y, Metzker ML, Allikmets R, Zack DJ, et al. 2001. A 5-bp deletion in ELOVL4 is associated with two related forms of autosomal dominant macular dystrophy. Nat Genet 27: 89-93.
177. Zhang F, Wang LP, Brauner M, Liewald JF, Kay K, Watzke N, Wood PG, Bamberg E, Nagel G, Gottschalk A, et al. 2007. Multimodal fast optical interrogation of neural circuitry. Nature 446: 633-639.
178. Zhao X, Liu J, Ahmad I. 2002. Differentiation of embryonic stem cells into retinal neurons. Biochem Biophys Res Commun 297: 177-184.
179. Zrenner E. 2002. Will retinal implants restore vision? Science 295: 1022-1025.
180. Zrenner E, Bartz-Schmidt KU, Benav H, Besch D, Bruck-mann A, Gabel VP, Gekeler F, Greppmaier U, Harscher A, Kibbel S, et al. 2011. Subretinal electronic chips allow blind patients to read letters and combine them to words. Proc Biol Sci 278: 1489-1497.