Spectral sensitivity measurements reveal partial success in restoring missing rod function with gene therapy

Journal of Vision

Volumn 15, Issue 15, 2015, Pages

  Ripamonti, Caterina ^a   Henning, G Bruce ^a   Robbie, Scott J ^a   Sundaram, Venki ^a   van den Born, L Ingeborgh ^b   Casteels, Ingele ^c   de Ravel, Thomy J L ^c   Moore, Anthony T ^a   Smith, Alexander J ^a   Bainbridge, James W ^a   Ali, Robin R ^a   Stockman, Andrew ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b ROTTERDAM EYE HOSPITAL   (Netherlands)

^c UNIVERSITY HOSPITALS LEUVEN   (Belgium)

Author keywords

Flicker sensitivity; Gene therapy; Rods and cones; RPE65; Scotopic; Temporal processing

Indexed keywords

CIS TRANS ISOMERASE; RETINOID ISOMEROHYDROLASE;

ADULT; CHILD; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; DARK ADAPTATION; DEPENDOPARVOVIRUS; GENE THERAPY; GENE VECTOR; GENETICS; HUMAN; LEBER CONGENITAL AMAUROSIS; LIGHT; MIDDLE AGED; PATHOPHYSIOLOGY; PHASE 1 CLINICAL TRIAL; PHASE 2 CLINICAL TRIAL; PHOTOSTIMULATION; PHYSIOLOGY; RETINA ROD; VISION; VISUAL ACUITY; VISUAL FIELD; YOUNG ADULT;

ADULT; CHILD; CIS-TRANS-ISOMERASES; DARK ADAPTATION; DEPENDOVIRUS; GENETIC THERAPY; GENETIC VECTORS; HUMANS; LEBER CONGENITAL AMAUROSIS; LIGHT; MIDDLE AGED; PHOTIC STIMULATION; RETINAL ROD PHOTORECEPTOR CELLS; VISION, OCULAR; VISUAL ACUITY; VISUAL FIELDS; YOUNG ADULT;

EID: 84950297196     PISSN: None     EISSN: 15347362     Source Type: Journal    
DOI: 10.1167/15.15.20     Document Type: Article

References (46)

1. Bainbridge, J.W. B., Mehat, M.S., Sundaram, V., Robbie, S.J., Barker, S.E., Ripamonti, C.,.. Ali, R.R. (2015). Long-term effect of gene therapy on Leber's congenital amaurosis. New England Journal of Medicine, 372, 1887-1897, doi:10.1056/ NEJMoa1414221.
2. Bainbridge, J.W. B., Smith, A.J., Barker, S.S., Robbie, S., Henderson, R., Balaggan, K.,.. Ali, R.R. (2008). Effect of gene therapy on visual function in Leber's congenital amaurosis. New England Journal of Medicine, 358, 1-9, doi:10.1056/ NEJMoa0802268.
3. Brown, T.M., Tsujimura, S., Allen, A.E., Wynne, J., Bedford, R., Vickery, G.,.. Lucas, R.J. (2012). Melanopsin-based brightness discrimination in mice and humans. Current Biology, 22, 1134-1141, doi:10.1016/j.cub.2012.04.039.
4. Burns, M.E., & Baylor, D.A. (2001). Activation, deactivation and adaptation in vertebrate photoreceptor cells. Annual Review of Neuroscience, 24, 779-805, doi:10.1146/annurev.neuro.24.1.779.
5. Cideciyan, A.V., Aleman, T.S., Boye, S.L., Schwartz, S.B., Kaushal, S., Roman, A.J.,.. Hauswirth, W.W. (2008). Human gene therapy for RPE65 isomerase deficiency activates the retinoid cycle of vision but with slow rod kinetics. Proceedings of the National Academy of Sciences, USA, 105, 15112-15117, doi:10.1073/pnas.0807027105.
6. Cideciyan, A.V., Hauswirth, W.W., Aleman, T.S., Kaushal, S., Schwartz, S.B., Boye, S.L.,.. Jacobson, S.G. (2009a). Human RPE65 gene therapy for Leber congenital amaurosis: persistence of early visual improvements and safety at 1 year. Human Gene Therapy, 20, 999-1004, doi:10.1089/ Hum.2009.086.
7. Cideciyan, A.V., Hauswirth, W.W., Aleman, T.S., Kaushal, S., Schwartz, S.B., Boye, S.L.,.. Jacobson, S.G. (2009b). Vision 1 Year after gene therapy for Leber's congenital amaurosis. New England Journal of Medicine, 361, 725-727, doi:10.1056/Nejmc0903652.
8. Commission Internationale de l' Eclairage. (1951). Commission Internationale de l' Eclairage Proceedings Stockholm. Paris: Bureau Central de la Commission Internationale de l'Eclairage.
9. Commission Internationale de l' Eclairage. (2006). Fundamental chromaticity diagram with physiological axes: Part 1. Technical Report 170-1. Vienna: Central Bureau of the Commission Internationale de l' Eclairage.
10. Doyle, S.E., Castrucci, A.M., McCall, M., Provencio, I., & Menaker, M. (2006). Nonvisual light responses in the Rpe65 knockout mouse: Rod loss restores sensitivity to the melanopsin system. Proceedings of the National Academy of Sciences, USA, 103, 10432-10437, doi:10.1073/pnas. 0600934103.
11. Fu, Y.B., Zhong, H.N., Wang, M.H. H., Luo, D.G., Liao, H.W., Maeda, H.,.. Yau, K.W. (2005). Intrinsically photosensitive retinal ganglion cells detect light with a vitamin A-based photopigment, melanopsin. Proceedings of the National Academy of Sciences, USA, 102, 10339-10344, doi:10.1073/ pnas.0501866102.
12. Gu, S.M., Thompson, D.A., Srikumari, C.R., Lorenz, B., Finckh, U., Nicoletti, A.,.. Gal, A. (1997). Mutations in RPE65 cause autosomal recessive childhood-onset severe retinal dystrophy Nature Genetics, 17, 194-197, doi:10.1038/ ng1097-194.
13. Hanein, S., Perrault, I., Gerber, S., Tanguy, G., Barbet, F., Ducroq, D.,.. Kaplan, J. (2004). Leber congenital amaurosis: Comprehensive survey of the genetic heterogeneity, refinement of the clinical definition, and genotype-phenotype correlations as a strategy for molecular diagnosis. Human Mutation, 23, 306-317, doi:10.1002/Humu.20010.
14. Hattar, S., Liao, H.W., Takao, M., Berson, D.M., & Yau, K.W. (2002). Melanopsin-containing retinal. ganglion cells: Architecture, projections, and intrinsic photosensitivity. Science, 295, 1065-1070, doi:10.1126/science.1069609.
15. Hauswirth, W.W., Aleman, T.S., Kaushal, S., Cideciyan, A.V., Schwartz, S.B., Wang, L.L.,.. Jacobson, S.G. (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. Human Gene Therapy, 19, 979-990, doi:10.1089/Hum.2008.107.
16. Horiguchi, H., Winawer, J., Dougherty, R.F., & Wandell, B.A. (2013). Human trichromacy revisited. Proceedings of the National Academy of Sciences, USA, 110, E260-E269, doi:10.1073/pnas. 1214240110.
17. Jacobson, S.G., Cideciyan, A.V., Ratnakaram, R., Heon, E., Schwartz, S.B., Roman, A.J.,.. Hauswirth, W.W. (2012). Gene therapy for Leber congenital amaurosis caused by RPE65 mutations: Safety and efficacy in fifteen children and adults followed up to three years. Archives of Ophthalmology, 130, 9-24.
18. Jin, M., Li, S., Moghrabi, W.N., Sun, H., & Travis, G.H. (2005). Rpe65 is the retinoid isomerase in bovine retinal pigment epithelium. Cell, 122, 449-459, doi: 10.1016/j.cell.2005.06.042.
19. Lamb, T.D. (1999). Photopigments and the biophysics of transduction in cone photoreceptors. In K. Gegenfurtner & L. T. Sharpe (Eds.), Color vision: From genes to perception (pp. 89-101). Cambridge: Cambridge University Press.
20. Lamb, T.D., & Pugh, E.N., Jr. (2004). Dark adaptation and the retinoid cycle of vision. Progress in Retinal and Eye Research, 23, 307-380, doi:10.1016/j.preteyeres.2004.03.001.
21. Lotery, A.J., Namperumalsamy, P., Jacobson, S.G., Weleber, R.G., Fishman, G.A., Musarella, M.A.,.. Stone, E.M. (2000). Mutation analysis of 3 genes in patients with Leber congenital amaurosis. Archives of Ophthalmology, 118, 538-543.
22. Maguire, A.M., Simonelli, F., Pierce, E.A., Pugh, E.N., Jr., Mingozzi, F., Bennicelli, J.,.. Bennett, J. (2008). Safety and efficacy of gene transfer for Leber's congenital amaurosis. New England Journal of Medicine, 358, 2240-2248, doi:10.1056/ NEJMoa0802315.
23. Marlhens, F., Bareil, C., Griffoin, J.M., Zrenner, E., Amalric, P., Eliaou, C.,.. Hamel, C.P. (1997). Mutations in RPE65 cause Leber's congenital amaurosis. Nature Genetics, 17, 139-141, doi:10.1038/Ng1097-139.
24. Mata, N.L., Moghrabi, W.N., Lee, J.S., Bui, T.V., Radu, R.A., Horwitz, J., & Travis, G.H. (2004). Rpe65 is a retinyl ester binding protein that presents insoluble substrate to the isomerase in retinal pigment epithelial cells. Journal of Biological Chemistry, 279, 635-643, doi:10.1074/jbc. M310042200.
25. Moiseyev, G., Chen, Y., Takahashi, Y., Wu, B.X., & Ma, J.X. (2005). RPE65 is the isomerohydrolase in the retinoid visual cycle. Proceedings of the National Academy of Sciences, USA, 102, 12413-12418, doi: 10.1073/pnas.0503460102.
26. Mowat, F.M., Breuwer, A.R., Bartoe, J.T., Annear, M.J., Zhang, Z., Smith, A.J.,.. Ali, R.R. (2013). RPE65 gene therapy slows cone loss in Rpe65-deficient dogs. Gene Therapy, 20, 545-555, doi:10.1038/gt.2012.63.
27. Mure, L.S., Rieux, C., Hattar, S., & Cooper, H.M. (2007). Melanopsin-dependent nonvisual responses: Evidence for photopigment bistability in vivo. Journal of Biological Rhythms, 22, 411-424, doi:10.1177/0748730407306043.
28. Perrault, I., Rozet, J.M., Gerber, S., Ghazi, I., Leowski, C., Ducroq, D.,.. Kaplan, J. (1999). Leber congenital amaurosis. Molecular Genetics and Metabolism, 68, 200-208.
29. Perrault, I., Rozet, J.M., Ghazi, I., Leowski, C., Bonnemaison, M., Gerber, M.,.. Kaplan, J. (1999). Different functional outcome of retGC1 and RPE65 gene mutations in Leber congenital amaurosis. American Journal of Human Genetics, 64, 1225-1228.
30. Provencio, I., Rodriguez, I.R., Jiang, G.S., Hayes, W.P., Moreira, E.F., & Rollag, M.D. (2000). A novel human opsin in the inner retina. Journal of Neuroscience, 20, 600-605.
31. Pugh, E.N., Jr. (1988). Vision: Physics and retinal physiology. In R. C. Atkinson, R.J. Herrnstein, G. Lindsey, & R. D. Luce (Eds.), Stevens' handbook of experimental psychology, second edition (Vol. 1, pp. 75-163). New York: Wiley.
32. Redmond, T.M., Poliakov, E., Yu, S., Tsai, J.Y., Lu, Z., & Gentleman, S. (2005). Mutation of key residues of RPE65 abolishes its enzymatic role as isomerohydrolase in the visual cycle. Proceedings of the National Academy of Sciences, USA, 102, 13658-13663, doi:10.1073/pnas.0504167102.
33. Redmond, T.M., Yu, S., Lee, E., Bok, D., Hamasaki, D., Chen, N.,.. Pfeifer, K. (1998). Rpe65 is necessary for production of 11-cis-vitamin A in the retinal visual cycle. Nature Genetics, 20, 344-351, doi:10.1038/3813.
34. Román, A.J., Cideciyan, A.V., Aleman, T.S., & Jacobson, S.G. (2007). Full-field stimulus testing (FST) to quantify visual perception in severely blind candidates for treatment trials. Physiological Measurement, 28, N51-N56, doi:10.1088/ 0967-3334/28/8/N02.
35. Sperling, H.G., & Harwerth, R.S. (1971). Red-green cone interactions in increment-threshold spectral sensitivity of primates. Science, 172, 180-184.
36. Stockman, A., & Sharpe, L.T. (2000). Spectral sensitivities of the middle- and long-wavelength sensitive cones derived from measurements in observers of known genotype. Vision Research, 40, 1711-1737.
37. Stockman, A., Sharpe, L.T., Tufail, A., Kell, P.D., Ripamonti, C., & Jeffery, G. (2007). The effect of sildenafil citrate (Viagrat) on visual sensitivity. Journal of Vision, 7(8):4, 1-15, doi:10.1167/7.8.4. [PubMed] [Article].
38. Stockman, A., Smithson, H.E., Michaelides, M., Moore, A.T., Webster, A.R., & Sharpe, L.T. (2007). Residual cone vision without a-transducin. Journal of Vision, 7(4):8, 1-13, doi:10.1167/7.4.8. [PubMed] [Article].
39. Stockman, A., Smithson, H.E., Webster, A.R., Holder, G.E., Rana, N.A., Ripamonti, C., & Sharpe, L.T. (2008). The loss of the PDE6 deactivating enzyme, RGS9, results in precocious light adaptation at low light levels. Journal of Vision, 8(1):10, 1-10. doi:10.1167/8.1.10. [PubMed] [Article].
40. Thompson, D.A., & Gal, A. (2003). Genetic defects in vitamin A metabolism of the retinal pigment epithelium. Developments in Ophthalmology, 37, 141-154.
41. Thompson, D.A., Gyurus, P., Fleischer, L.L., Bingham, E.L., McHenry, C.L., Apfelstedt-Sylla, E.,.. Gal, A. (2000). Genetics and phenotypes of RPE65 mutations in inherited retinal degeneration. Investigative Ophthalmology & Visual Science, 41, 4293-4299. [PubMed] [Article].
42. Tu, D.C., Owens, L.A., Anderson, L., Golczak, M., Doyle, S.E., McCall, M.,.. Van Gelder, R.N. (2006). Inner retinal photoreception independent of the visual retinoid cycle. Proceedings of the National Academy of Sciences, USA, 103, 10426-10431, doi: 10.1073/pnas.0600917103.
43. Wong, K.Y., Dunn, F.A., & Berson, D.M. (2005). Photoreceptor adaptation in intrinsically photosensitive retinal ganglion cells. Neuron, 48, 1001-1010, doi:10.1016/j.neuron.2005.11.016.
44. Wu, B.X., Moiseyev, G., Chen, Y., Rohrer, B., Crouch, R.K., & Ma, J.X. (2004). Identification of RDH10, an all-trans retinol dehydrogenase, in retinal Muller cells. Investigative Ophthalmology & Visual Science, 45, 3857-3862. [PubMed] [Article].
45. Zaidi, F.H., Hull, J.T., Peirson, S.N., Wulff, K., Aeschbach, D., Gooley, J.J.,.. Lockley, S.W. (2007). Short-wavelength light sensitivity of circadian, pupillary, and visual awareness in humans lacking an outer retina. Current Biology, 17, 2122-2128, doi:10.1016/j.cub.2007.11.034.
46. Znoiko, S.L., Crouch, R.K., Moiseyev, G., & Ma, J.X. (2002). Identification of the RPE65 protein in mammalian cone photoreceptors. Investigative Ophthalmology & Visual Science, 43, 1604-1609. [PubMed] [Article].