Successful gene therapy in the RPGRIP1-deficient dog: A large model of cone-rod dystrophy

Molecular Therapy

Volumn 22, Issue 2, 2014, Pages 265-277

  Lhériteau, Elsa ^a   Petit, Lolita ^a   Weber, Michel ^b   Le Meur, Guylène ^b   Deschamps, Jack Yves ^c   Libeau, Lyse ^a   Mendes Madeira, Alexandra ^a   Guihal, Caroline ^a   François, Achille ^a   Guyon, Richard ^d   Provost, Nathalie ^a   Lemoine, Françoise ^e   Papal, Samantha ^f   El Amraoui, Aziz ^f   Colle, Marie Anne ^c   Moullier, Philippe ^a,g   Rolling, Fabienne ^a  

^a UNIVERSITÉ DE NANTES   (France)

^b HÔTEL DIEU   (France)

^c LUNAM UNIVERSITÉ   (France)

^d UNIVERSITÉ DE RENNES 1   (France)

^e CLINIQUE VÉTÉRINAIRE   (France)

^f INSTITUT PASTEUR   (France)

^g UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CLINICAL EFFECTIVENESS; CONTROLLED STUDY; DOG; GENE REPLACEMENT THERAPY; GENE TRANSFER; NONHUMAN; RETINA CONE; RETINA CONE ROD DYSTROPHY; RETINA DEGENERATION; RETINA DYSTROPHY; RETINA ROD; VISION; VISUAL IMPAIRMENT; ADMINISTRATION AND DOSAGE; ANIMAL; DEPENDOPARVOVIRUS; DISEASE COURSE; DISEASE MODEL; GENE EXPRESSION; GENE INACTIVATION; GENE ORDER; GENE THERAPY; GENE VECTOR; GENETIC TRANSDUCTION; GENETICS; HUMAN; METABOLISM; PATHOLOGY; PROMOTER REGION; REPORTER GENE; RETINITIS PIGMENTOSA; TRANSGENIC ANIMAL; TREATMENT OUTCOME;

ANIMALIA; CANIS FAMILIARIS;

ENHANCED GREEN FLUORESCENT PROTEIN; EYE PROTEIN; GREEN FLUORESCENT PROTEIN;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; DEPENDOVIRUS; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; DOGS; EYE PROTEINS; GENE EXPRESSION; GENE KNOCKOUT TECHNIQUES; GENE ORDER; GENE TRANSFER TECHNIQUES; GENES, REPORTER; GENETIC THERAPY; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; HUMANS; PROMOTER REGIONS, GENETIC; RETINAL CONE PHOTORECEPTOR CELLS; RETINAL ROD PHOTORECEPTOR CELLS; RETINITIS PIGMENTOSA; TRANSDUCTION, GENETIC; TREATMENT OUTCOME;

EID: 84895905784     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2013.232     Document Type: Article

References (50)

1. Hartong, DT, Berson, EL and Dryja, TP (2006). Retinitis pigmentosa. Lancet 368: 1795-1809.
2. Michaelides, M, Hardcastle, AJ, Hunt, DM and Moore, AT (2006). Progressive cone and cone-rod dystrophies: phenotypes and underlying molecular genetic basis. Surv Ophthalmol 51: 232-258.
3. Hamel, CP (2007). Cone rod dystrophies. Orphanet J Rare Dis 2: 7.
4. den Hollander, AI, Black, A, Bennett, J and Cremers, FP (2010). Lighting a candle in the dark: advances in genetics and gene therapy of recessive retinal dystrophies. J Clin Invest 120: 3042-3053.
5. Smith, AJ, Bainbridge, JW and Ali, RR (2012). Gene supplementation therapy for recessive forms of inherited retinal dystrophies. Gene Ther 19: 154-161.
6. Colella, P and Auricchio, A (2012). Gene therapy of inherited retinopathies: a long and successful road from viral vectors to patients. Hum Gene Ther 23: 796-807.
7. Boye, SE, Boye, SL, Lewin, AS and Hauswirth, WW (2013). A comprehensive review of retinal gene therapy. Mol Ther 21: 509-519.
8. Stieger, K, Lhériteau, E, Lhéariteau, E, Moullier, P and Rolling, F (2009). AAV-mediated gene therapy for retinal disorders in large animal models. ILAR J 50: 206-224.
9. Komáromy, AM, Alexander, JJ, Rowlan, JS, Garcia, MM, Chiodo, VA, Kaya, A et al. (2010). Gene therapy rescues cone function in congenital achromatopsia. Hum Mol Genet 19: 2581-2593.
10. Petit, L, Lhériteau, E, Weber, M, Le Meur, G, Deschamps, JY, Provost, N et al. (2012). Restoration of vision in the pde6®-deficient dog, a large animal model of rod-cone dystrophy. Mol Ther 20: 2019-2030.
11. Beltran, WA, Cideciyan, AV, Lewin, AS, Iwabe, S, Khanna, H, Sumaroka, A et al. (2012). Gene therapy rescues photoreceptor blindness in dogs and paves the way for treating human X-linked retinitis pigmentosa. Proc Natl Acad Sci USA 109: 2132-2137.
12. Turney, C, Chong, NH, Alexander, RA, Hogg, CR, Fleming, L, Flack, D et al. (2007). Pathological and electrophysiological features of a canine cone-rod dystrophy in the miniature longhaired dachshund. Invest Ophthalmol Vis Sci 48: 4240-4249.
13. Lhériteau, E, Libeau, L, Stieger, K, Deschamps, JY, Mendes-Madeira, A, Provost, N et al. (2009). The RPGRIP1-deficient dog, a promising canine model for gene therapy. Mol Vis 15: 349-361.
14. Mellersh, CS, Boursnell, ME, Pettitt, L, Ryder, EJ, Holmes, NG, Grafham, D et al. (2006). Canine RPGRIP1 mutation establishes cone-rod dystrophy in miniature longhaired dachshunds as a homologue of human Leber congenital amaurosis. Genomics 88: 293-301.
15. Dryja, TP, Adams, SM, Grimsby, JL, McGee, TL, Hong, DH, Li, T et al. (2001). Null RPGRIP1 alleles in patients with Leber congenital amaurosis. Am J Hum Genet 68: 1295-1298.
16. Gerber, S, Perrault, I, Hanein, S, Barbet, F, Ducroq, D, Ghazi, I et al. (2001). Complete exon-intron structure of the RPGR-interacting protein (RPGRIP1) gene allows the identification of mutations underlying Leber congenital amaurosis. Eur J Hum Genet 9: 561-571.
17. Jacobson, SG, Cideciyan, AV, Aleman, TS, Sumaroka, A, Schwartz, SB, Roman, AJ et al. (2007). Leber congenital amaurosis caused by an RPGRIP1 mutation shows treatment potential. Ophthalmology 114: 895-898.
18. Fakhratova, M (2013). Identification of a novel LCA6 mutation in an Emirati family. Ophthalmic Genet, published online 2 January 2013 (doi:10.3109/13816810.2012.75 5552).
19. Khan, AO, Abu-Safieh, L, Eisenberger, T, Bolz, HJ and Alkuraya, FS (2013). The RPGRIP1-related retinal phenotype in children. Br J Ophthalmol 97: 760-764.
20. Hameed, A, Abid, A, Aziz, A, Ismail, M, Mehdi, SQ and Khaliq, S (2003). Evidence of RPGRIP1 gene mutations associated with recessive cone-rod dystrophy. J Med Genet 40: 616-619.
21. Roepman, R, Bernoud-Hubac, N, Schick, DE, Maugeri, A, Berger, W, Ropers, HH et al. (2000). The retinitis pigmentosa GTPase regulator (RPGR) interacts with novel transport-like proteins in the outer segments of rod photoreceptors. Hum Mol Genet 9: 2095-2105.
22. Hong, DH, Yue, G, Adamian, M and Li, T (2001). Retinitis pigmentosa GTPase regulator (RPGRr)-interacting protein is stably associated with the photoreceptor ciliary axoneme and anchors RPGR to the connecting cilium. J Biol Chem 276: 12091-12099.
23. Mavlyutov, TA, Zhao, H and Ferreira, PA (2002). Species-specific subcellular localization of RPGR and RPGRIP isoforms: implications for the phenotypic variability of congenital retinopathies among species. Hum Mol Genet 11: 1899-1907.
24. Boylan, JP and Wright, AF (2000). Identification of a novel protein interacting with RPGR. Hum Mol Genet 9: 2085-2093.
25. Zhao, Y, Hong, DH, Pawlyk, B, Yue, G, Adamian, M, Grynberg, M et al. (2003). The retinitis pigmentosa GTPase regulator (RPGR)- interacting protein: subserving RPGR function and participating in disk morphogenesis. Proc Natl Acad Sci USA 100: 3965-3970.
26. Won, J, Gifford, E, Smith, RS, Yi, H, Ferreira, PA, Hicks, WL et al. (2009). RPGRIP1 is essential for normal rod photoreceptor outer segment elaboration and morphogenesis. Hum Mol Genet 18: 4329-4339.
27. Pawlyk, BS, Smith, AJ, Buch, PK, Adamian, M, Hong, DH, Sandberg, MA et al. (2005). Gene replacement therapy rescues photoreceptor degeneration in a murine model of Leber congenital amaurosis lacking RPGRIP. Invest Ophthalmol Vis Sci 46: 3039-3045.
28. Pawlyk, BS, Bulgakov, OV, Liu, X, Xu, X, Adamian, M, Sun, X et al. (2010). Replacement gene therapy with a human RPGRIP1 sequence slows photoreceptor degeneration in a murine model of Leber congenital amaurosis. Hum Gene Ther 21: 993-1004.
29. Le Meur, G, Weber, M, Péréon, Y, Mendes-Madeira, A, Nivard, D, Deschamps, JY et al. (2005). Postsurgical assessment and long-term safety of recombinant adenoassociated virus-mediated gene transfer into the retinas of dogs and primates. Arch Ophthalmol 123: 500-506.
30. Mussolino, C, della Corte, M, Rossi, S, Viola, F, Di Vicino, U, Marrocco, E et al. (2011). AAV-mediated photoreceptor transduction of the pig cone-enriched retina. Gene Ther 18: 637-645.
31. Vandenberghe, LH, Bell, P, Maguire, AM, Cearley, CN, Xiao, R, Calcedo, R et al. (2011). Dosage thresholds for AAV2 and AAV8 photoreceptor gene therapy in monkey. Sci Transl Med 3: 88ra54.
32. Boye, SE, Alexander, JJ, Boye, SL, Witherspoon, CD, Sandefer, KJ, Conlon, TJ 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: 1101-1115.
33. Khani, SC, Pawlyk, BS, Bulgakov, OV, Kasperek, E, Young, JE, Adamian, M et al. (2007). AAV-mediated expression targeting of rod and cone photoreceptors with a human rhodopsin kinase promoter. Invest Ophthalmol Vis Sci 48: 3954-3961.
34. Sun, X, Pawlyk, B, Xu, X, Liu, X, Bulgakov, OV, Adamian, M et al. (2010). Gene therapy with a promoter targeting both rods and cones rescues retinal degeneration caused by AIPL1 mutations. Gene Ther 17: 117-131.
35. Ku, CA, Chiodo, VA, Boye, SL, Goldberg, AF, Li, T, Hauswirth, WW et al. (2011). Gene therapy using self-complementary Y733F capsid mutant AAV2/8 restores vision in a model of early onset Leber congenital amaurosis. Hum Mol Genet 20: 4569-4581.
36. Boye, SE, Boye, SL, Pang, J, Ryals, R, Everhart, D, Umino, Y et al. (2010). Functional and behavioral restoration of vision by gene therapy in the guanylate cyclase-1 (GC1) knockout mouse. PLoS ONE 5: e11306.
37. Mihelec, M, Pearson, RA, Robbie, SJ, Buch, PK, Azam, SA, Bainbridge, JW 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: 1179-1190.
38. Boye, SL, Peshenko, IV, Huang, WC, Min, SH, McDoom, I, Kay, CN et al. (2013). AAVmediated gene therapy in the guanylate cyclase (RetGC1/RetGC2) double knockout mouse model of Leber congenital amaurosis. Hum Gene Ther 24: 189-202.
39. Beltran, WA, Boye, SL, Boye, SE, Chiodo, VA, Lewin, AS, Hauswirth, WW et al. (2010). rAAV2/5 gene-targeting to rods:dose-dependent efficiency and complications associated with different promoters. Gene Ther 17: 1162-1174.
40. Kuznetsova, T, Zangerl, B, Goldstein, O, Acland, GM and Aguirre, GD (2011). Structural organization and expression pattern of the canine RPGRIP1 isoforms in retinal tissue. Invest Ophthalmol Vis Sci 52: 2989-2998.
41. Miyadera, K, Kato, K, Boursnell, M, Mellersh, CS and Sargan, DR (2012). Genomewide association study in RPGRIP1(-/-) dogs identifies a modifier locus that determines the onset of retinal degeneration. Mamm Genome 23: 212-223.
42. Kuznetsova, T, Iwabe, S, Boesze-Battaglia, K, Pearce-Kelling, S, Chang-Min, Y, McDaid, K et al. (2012). Exclusion of RPGRIP1 ins44 from primary causal association with early-onset cone-rod dystrophy in dogs. Invest Ophthalmol Vis Sci 53: 5486-5501.
43. Miyadera, K, Brierley, I, Aguirre-Hernández, J, Mellersh, CS and Sargan, DR (2012). Multiple mechanisms contribute to leakiness of a frameshift mutation in canine conerod dystrophy. PLoS ONE 7: e51598.
44. Boye, SL, Conlon, T, Erger, K, Ryals, R, Neeley, A, Cossette, T et al. (2011). Longterm preservation of cone photoreceptors and restoration of cone function by gene therapy in the guanylate cyclase-1 knockout (GC1KO) mouse. Invest Ophthalmol Vis Sci 52: 7098-7108.
45. Tan, MH, Smith, AJ, Pawlyk, B, Xu, X, Liu, X, Bainbridge, JB 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: 2099-2114.
46. Simons, DL, Boye, SL, Hauswirth, WW and Wu, SM (2011). Gene therapy prevents photoreceptor death and preserves retinal function in a Bardet-Biedl syndrome mouse model. Proc Natl Acad Sci USA 108: 6276-6281.
47. Cideciyan, AV, Jacobson, SG, Beltran, WA, Sumaroka, A, Swider, M, Iwabe, S et al. (2013). Human retinal gene therapy for Leber congenital amaurosis shows advancing retinal degeneration despite enduring visual improvement. Proc Natl Acad Sci USA 110: E517-E525.
48. Acland, GM, Aguirre, GD, Bennett, J, Aleman, TS, Cideciyan, AV, Bennicelli, J 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.
49. Koch, S, Sothilingam, V, Garcia Garrido, M, Tanimoto, N, Becirovic, E, Koch, F et al. (2012). Gene therapy restores vision and delays degeneration in the CNGB1(-/-) mouse model of retinitis pigmentosa. Hum Mol Genet 21: 4486-4496.
50. Pang, JJ, Dai, X, Boye, SE, Barone, I, Boye, SL, Mao, S et al. (2011). Longterm retinal function and structure rescue using capsid mutant AAV8 vector in the rd10 mouse, a model of recessive retinitis pigmentosa. Mol Ther 19: 234-242.