A long-term efficacy study of gene replacement therapy for RPGR-associated retinal degeneration

Human Molecular Genetics

Volumn 24, Issue 14, 2015, Pages 3956-3970

  Wu, Zhijian ^a   Hiriyanna, Suja ^a   Qian, Haohua ^a   Mookherjee, Suddhasil ^a   Campos, Maria M ^a   Gao, Chun ^a   Fariss, Robert ^a   Sieving, Paul A ^a   Li, Tiansen ^a   Colosi, Peter ^a   Swaroop, Anand ^a  

^a NATIONAL EYE INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

OPSIN; PARVOVIRUS VECTOR; REGULATOR PROTEIN; RETINITIS PIGMENTOSA GUANOSINE TRIPHOSPHATASE REGULATOR; UNCLASSIFIED DRUG; CARRIER PROTEIN; EYE PROTEIN; RPGR PROTEIN, HUMAN; RPGR PROTEIN, MOUSE;

AGE; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ELECTRORETINOGRAM; GENE DOSAGE; GENE EXPRESSION; GENE REPLACEMENT THERAPY; GENE TARGETING; HUMAN; MOUSE; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA; RETINITIS PIGMENTOSA; VIRAL GENE THERAPY; ANIMAL; C57BL MOUSE; DEPENDOPARVOVIRUS; DISEASE MODEL; ELECTRORETINOGRAPHY; EXON; GENE THERAPY; GENE VECTOR; GENETICS; KNOCKOUT MOUSE; MALE; METABOLISM; MUTATION; OPEN READING FRAME;

CANIS FAMILIARIS; MUS;

ANIMALS; CARRIER PROTEINS; DEPENDOVIRUS; DISEASE MODELS, ANIMAL; ELECTRORETINOGRAPHY; EXONS; EYE PROTEINS; GENETIC THERAPY; GENETIC VECTORS; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUTATION; OPEN READING FRAMES; RETINA; RETINITIS PIGMENTOSA;

EID: 84936745091     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddv134     Document Type: Article

References (50)

1. Hartong, D.T., Berson, E.L. and Dryja, T.P. (2006) Retinitis pigmentosa. Lancet, 368, 1795-1809.
2. Vervoort, R., Lennon, A., Bird, A.C., Tulloch, B., Axton, R., Miano, M.G., Meindl, A., Meitinger, T., Ciccodicola, A. and Wright, A.F. (2000) Mutational hot spot within a new RPGR exon in X-linked retinitis pigmentosa. Nat. Genet., 25, 462-466.
3. Sharon, D., Sandberg, M.A., Rabe, V.W., Stillberger, M., Dryja, T.P. and Berson, E.L. (2003) RP2 and RPGR mutations and clinical correlations in patients with X-linked retinitis pigmentosa. Am. J. Hum. Genet., 73, 1131-1146.
4. Pelletier, V., Jambou, M., Delphin, N., Zinovieva, E., Stum, M., Gigarel, N., Dollfus, H., Hamel, C., Toutain, A., Dufier, J.L. et al. (2007) Comprehensive survey of mutations in RP2 and RPGR in patients affected with distinct retinal dystrophies: genotype-phenotype correlations and impact on genetic counseling. Hum. Mutat., 28, 81-91.
5. Shu, X., McDowall, E., Brown, A.F. andWright, A.F. (2008) The human retinitis pigmentosa GTPase regulator gene variant database. Hum. Mutat., 29, 605-608.
6. Branham, K., Othman, M., Brumm, M., Karoukis, A.J., Atmaca-Sonmez, P., Yashar, B.M., Schwartz, S.B., Stover, N.B., Trzupek, K., Wheaton, D. et al. (2012) Mutations in RPGR and RP2 account for 15% of males with simplex retinal degenerative disease. Invest. Ophthalmol. Vis. Sci., 53, 8232-8237.
7. Churchill, J.D., Bowne, S.J., Sullivan, L.S., Lewis, R.A., Wheaton, D.K., Birch, D.G., Branham, K.E., Heckenlively, J.R. and Daiger, S.P. (2013) Mutations in the X-linked retinitis pigmentosa genes RPGR and RP2 found in 8.5% of families with a provisional diagnosis of autosomal dominant retinitis pigmentosa. Invest. Ophthalmol. Vis. Sci., 54, 1411-1416.
8. Sullivan, L.S., Bowne, S.J., Reeves, M.J., Blain, D., Goetz, K., Ndifor, V., Vitez, S., Wang, X., Tumminia, S.J. and Daiger, S.P. (2013) Prevalence of mutations in eyeGENE probands with a diagnosis of autosomal dominant retinitis pigmentosa. Invest. Ophthalmol. Vis. Sci., 54, 6255-6261.
9. Bowne, S.J., Sullivan, L.S., Koboldt, D.C., Ding, L., Fulton, R., Abbott, R.M., Sodergren, E.J., Birch, D.G., Wheaton, D.H., Heckenlively, J.R. et al. (2011) Identification of disease-causing mutations in autosomal dominant retinitis pigmentosa (adRP) using next-generation DNA sequencing. Invest. Ophthalmol. Vis. Sci., 52, 494-503.
10. Yan, D., Swain, P.K., Breuer, D., Tucker, R.M., Wu, W., Fujita, R., Rehemtulla, A., Burke, D. and Swaroop, A. (1998) Biochemical characterization and subcellular localization of the mouse retinitis pigmentosa GTPase regulator (mRpgr). J. Bio. Chem., 273, 19656-19663.
11. Kirschner, R., Rosenberg, T., Schultz-Heienbrok, R., Lenzner, S., Feil, S., Roepman, R., Cremers, F.P., Ropers, H.H. and Berger, W. (1999) RPGR transcription studies in mouse and human tissues reveal a retina-specific isoform that is disrupted in a patient with X-linked retinitis pigmentosa. Hum. Mol. Genet., 8, 1571-1578.
12. Hong, D.H. and Li, T. (2002) Complex expression pattern of RPGR reveals a role for purine-rich exonic splicing enhancers. Invest. Ophthalmol. Vis. Sci., 43, 3373-3382.
13. Rachel, R.A., Li, T. and Swaroop, A. (2012) Photoreceptor sensory cilia and ciliopathies: focus on CEP290, RPGR and their interacting proteins. Cilia, 1, 22.
14. Hong, D.H., Pawlyk, B.S., Shang, J., Sandberg, M.A., Berson, E.L. and Li, T. (2000) A retinitis pigmentosa GTPase regulator (RPGR)-deficient mouse model for X-linked retinitis pigmentosa (RP3). Proc. Natl Acad. Sci., 97, 3649-3654.
15. Hong, D.H., Pawlyk, B., Sokolov, M., Strissel, K.J., Yang, J., Tulloch, B., Wright, A.F., Arshavsky, V.Y. and Li, T. (2003) RPGR isoforms in photoreceptor connecting cilia and the transitional zone of motile cilia. Invest. Ophthalmol. Vis. Sci., 44, 2413-2421.
16. Hosch, J., Lorenz, B. and Stieger, K. (2011) RPGR: role in the photoreceptor cilium, human retinal disease, and gene therapy. Ophthalmic Genet., 32, 1-11.
17. Brunner, S., Skosyrski, S., Kirschner-Schwabe, R., Knobeloch, K.P., Neidhardt, J., Feil, S., Glaus, E., Luhmann, U.F., Ruther, K. and Berger, W. (2010) Cone versus rod disease in a mutant Rpgr mouse caused by different genetic backgrounds. Invest. Ophthalmol. Vis. Sci., 51, 1106-1115.
18. Thompson, D.A., Khan, N.W., Othman, M.I., Chang, B., Jia, L., Grahek, G., Wu, Z., Hiriyanna, S., Nellissery, J., Li, T. et al. (2012) Rd9 is a naturally occurring mouse model of a common form of retinitis pigmentosa caused by mutations in RPGR-ORF15. PloS One, 7, e35865.
19. Adamian, M., Pawlyk, B.S., Hong, D.H. and Berson, E.L. (2006) Rod and cone opsin mislocalization in an autopsy eye from a carrier of X-linked retinitis pigmentosa with a Gly436Asp mutation in the RPGR gene. Am. J. Ophthal., 142, 515-518.
20. Boye, S.E., Boye, S.L., Lewin, A.S. and Hauswirth, W.W. (2013) A comprehensive review of retinal gene therapy. Mol. Ther., 21, 509-519.
21. Maguire, A.M., Simonelli, F., Pierce, E.A., Pugh, E.N. Jr., Mingozzi, F., Bennicelli, J., Banfi, S., Marshall, K.A., Testa, F., Surace, E.M. et al. (2008) Safety and efficacy of gene transfer for Leber's congenital amaurosis. N. Eng. J. Med., 358, 2240-2248.
22. Bainbridge, J.W., Smith, A.J., Barker, S.S., Robbie, S., Henderson, R., Balaggan, K., Viswanathan, A., Holder, G.E., Stockman, A., Tyler, N. et al. (2008) Effect of gene therapy on visual function in Leber's congenital amaurosis. N. Eng. J. Med., 358, 2231-2239.
23. Cideciyan, A.V., Aleman, T.S., Boye, S.L., Schwartz, S.B., Kaushal, S., Roman, A.J., Pang, J.J., Sumaroka, A., Windsor, E.A., Wilson, J.M. et al. (2008) Human gene therapy for RPE65 isomerase deficiency activates the retinoid cycle of vision but with slow rod kinetics. Proc. Natl Acad. Sci., 105, 15112-15117.
24. Simonelli, F., Maguire, A.M., Testa, F., Pierce, E.A., Mingozzi, F., Bennicelli, J.L., Rossi, S., Marshall, K., Banfi, S., Surace, E.M. et al. (2010) Gene therapy for Leber's congenital amaurosis is safe and effective through 1.5 years after vector administration. Mol. Ther., 18, 643-650.
25. Maguire, A.M., High, K.A., Auricchio, A., Wright, J.F., Pierce, E.A., Testa, F., Mingozzi, F., Bennicelli, J.L., Ying, G.S., Rossi, S. et al. (2009) Age-dependent effects of RPE65 gene therapy for Leber's congenital amaurosis: a phase 1 dose-escalation trial. Lancet, 374, 1597-1605.
26. Bennett, J., Ashtari, M., Wellman, J., Marshall, K.A., Cyckowski, L.L., Chung, D.C., McCague, S., Pierce, E.A., Chen, Y., Bennicelli, J.L. et al. (2012) AAV2 gene therapy readministration in three adults with congenital blindness. Sci. Transl. Med., 4, 120ra115.
27. Jacobson, S.G., Cideciyan, A.V., Ratnakaram, R., Heon, E., Schwartz, S.B., Roman, A.J., Peden, M.C., Aleman, T.S., Boye, S.L., 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. Ophthal., 130, 9-24.
28. Cideciyan, A.V., Hauswirth, W.W., Aleman, T.S., Kaushal, S., Schwartz, S.B., Boye, S.L., Windsor, E.A., Conlon, T.J., Sumaroka, A., Pang, J.J. et al. (2009) Human RPE65 gene therapy for Leber congenital amaurosis: persistence of early visual improvements and safety at 1 year. Hum. Gene Ther., 20, 999-1004.
29. MacLaren, R.E., Groppe, M., Barnard, A.R., Cottriall, C.L., Tolmachova, T., Seymour, L., Clark, K.R., During, M.J., Cremers, F.P., Black, G.C. et al. (2014) Retinal gene therapy in patients with choroideremia: initial findings from a phase 1/2 clinical trial. Lancet, 383, 1129-1137.
30. Lam, B.L., Feuer, W.J., Schiffman, J.C., Porciatti, V., Vandenbroucke, R., Rosa, P.R., Gregori, G. and Guy, J. (2014) Trial end points and natural history in patients with G11778A Leber hereditary optic neuropathy: preparation for gene therapy clinical trial. JAMA Ophthal., 132, 428-436.
31. Lheriteau, E., Petit, L., Weber, M., Le Meur, G., Deschamps, J.Y., Libeau, L., Mendes-Madeira, A., Guihal, C., Francois, A., Guyon, R. et al. (2014) Successful gene therapy in the RPGRIP1-deficient dog: a large model of cone-rod dystrophy. Mol. Ther., 22, 265-277.
32. Lai, C.M., Estcourt, M.J., Himbeck, R.P., Lee, S.Y., Yew-San Yeo, I., Luu, C., Loh, B.K., Lee, M.W., Barathi, A., Villano, J. et al. (2012) Preclinical safety evaluation of subretinal AAV2.sFlt-1 in non-human primates. Gene Ther., 19, 999-1009.
33. Binley, K., Widdowson, P., Loader, J., Kelleher, M., Iqball, S., Ferrige, G., de Belin, J., Carlucci, M., Angell-Manning, D., Hurst, F. et al. (2013) Transduction of photoreceptors with equine infectious anemia virus lentiviral vectors: safety and biodistribution of StarGen for Stargardt disease. Invest. Ophthalmol. Vis. Sci., 54, 4061-4071.
34. Zhang, Q., Acland, G.M., Wu, W.X., Johnson, J.L., Pearce-Kelling, S., Tulloch, B., Vervoort, R., Wright, A.F. and Aguirre, G. D. (2002) Different RPGR exon ORF15 mutations in Canids provide insights into photoreceptor cell degeneration. Hum. Mol. Genet., 11, 993-1003.
35. Huang, W.C., Wright, A.F., Roman, A.J., Cideciyan, A.V., Manson, F.D., Gewaily, D.Y., Schwartz, S.B., Sadigh, S., Limberis, M.P., Bell, P. et al. (2012) RPGR-associated retinal degeneration in human X-linked RP and a murine model. Invest. Ophthalmol. Vis. Sci., 53, 5594-5608.
36. Hong, D.H., Pawlyk, B.S., Adamian, M., Sandberg, M.A. and Li, T. (2005) A single, abbreviated RPGR-ORF15 variant reconstitutes RPGR function in vivo. Invest. Ophthalmol. Vis. Sci., 46, 435-441.
37. Wright, R.N., Hong, D.H. and Perkins, B. (2011) Misexpression of the constitutive Rpgr(ex1-19) variant leads to severe photoreceptor degeneration. Invest. Ophthalmol. Vis. Sci., 52, 5189-5201.
38. Beltran, W.A., Cideciyan, A.V., Lewin, A.S., Iwabe, S., Khanna, H., Sumaroka, A., Chiodo, V.A., Fajardo, D.S., Roman, A.J., Deng, W.T. et al. (2012) Gene therapy rescues photoreceptor blindness in dogs and paves the way for treating human Xlinked retinitis pigmentosa. Proc. Natl Acad. Sci., 109, 2132-2137.
39. Allocca, M., Mussolino, C., Garcia-Hoyos, M., Sanges, D., Iodice, C., Petrillo, M., Vandenberghe, L.H., Wilson, J.M., Marigo, V., Surace, E.M. et al. (2007) Novel adeno-associated virus serotypes efficiently transduce murine photoreceptors. J. Virol., 81, 11372-11380.
40. Vandenberghe, L.H., Bell, P., Maguire, A.M., Cearley, C.N., Xiao, R., Calcedo, R., Wang, L., Castle, M.J., Maguire, A.C., Grant, R. et al. (2011) Dosage thresholds for AAV2 and AAV8 photoreceptor gene therapy in monkey. Sci. Transl. Med., 3, 88ra54.
41. Vandenberghe, L.H., Bell, P., Maguire, A.M., Xiao, R., Hopkins, T.B., Grant, R., Bennett, J. andWilson, J.M. (2013) AAV9 targets cone photoreceptors in the nonhuman primate retina. PLoS One, 8, e53463.
42. Khani, S.C., Pawlyk, B.S., Bulgakov, O.V., Kasperek, E., Young, J.E., Adamian, M., Sun, X., Smith, A.J., Ali, R.R. and Li, T. (2007) AAV-mediated expression targeting of rod and cone photoreceptors with a human rhodopsin kinase promoter. Invest. Ophthalmol. Vis. Sci., 48, 3954-3961.
43. Sun, X., Pawlyk, B., Xu, X., Liu, X., Bulgakov, O.V., Adamian, M., Sandberg, M.A., Khani, S.C., Tan, M.H., Smith, A.J. 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.
44. Tan, M.H., Smith, A.J., Pawlyk, B., Xu, X., Liu, X., Bainbridge, J.B., Basche, M., McIntosh, J., Tran, H.V., Nathwani, A. 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.
45. Cideciyan, A.V., Jacobson, S.G., Beltran, W.A., Sumaroka, A., Swider, M., Iwabe, S., Roman, A.J., Olivares, M.B., Schwartz, S.B., Komaromy, A.M. 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.
46. Schnepp, B.C., Jensen, R.L., Chen, C.L., Johnson, P.R. and Clark, K.R. (2005) Characterization of adeno-associated virus genomes isolated from human tissues. J. Virol., 79, 14793-14803.
47. Grimm, D., Pandey, K., Nakai, H., Storm, T.A. and Kay, M.A. (2006) Liver transduction with recombinant adeno-associated virus is primarily restricted by capsid serotype not vector genotype. J. Virol., 80, 426-439.
48. Penaud-Budloo, M., Le Guiner, C., Nowrouzi, A., Toromanoff, A., Chérel, Y., Chenuaud, P., Schmidt, M., von Kalle, C., Rolling, F., Moullier, P. and Snyder, R.O. (2008) Adeno-associated virus vector genomes persist as episomal chromatin in primate muscle. J. Virol., 82, 7875-7885.
49. Park, T.K., Wu, Z., Kjellstrom, S., Zeng, Y., Bush, R.A., Sieving, P.A. and 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.
50. Grimm, D., Zhou, S., Nakai, H., Thomas, C.E., Storm, T.A., Fuess, S., Matsushita, T., Allen, J., Surosky, R., Lochrie, M. et al. (2003) Preclinical in vivo evaluation of pseudotyped adeno-associated virus vectors for liver gene therapy. Blood, 102, 2412-2419.