AAV-mediated gene therapy halts retinal degeneration in PDE6β-deficient dogs

Molecular Therapy

Volumn 24, Issue 5, 2016, Pages 867-876

  Pichard, Virginie ^a   Provost, Nathalie ^a   Mendes Madeira, Alexandra ^a   Libeau, Lyse ^a   Hulin, Philippe ^a   Tshilenge, Kizito Tshitoko ^a   Biget, Marine ^a   Ameline, Baptiste ^a   Deschamps, Jack Yves ^b   Weber, Michel ^c   Le Meur, Guylene ^c   Colle, Marie Anne ^b   Moullier, Philippe ^a,d   Rolling, Fabienne ^a  

^a UNIVERSITÉ DE NANTES   (France)

^b LUNAM UNIVERSITÉ   (France)

^c NANTES UNIVERSITY HOSPITAL   (France)

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

Author keywords

[No Author keywords available]

Indexed keywords

PARVOVIRUS VECTOR; PHOSPHODIESTERASE VI; PHOSPHODIESTERASE VI BETA; UNCLASSIFIED DRUG;

ADENO ASSOCIATED VIRUS 2; ADENO ASSOCIATED VIRUS 5; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOG; HETEROZYGOTE; NONHUMAN; PDE6BETA GENE; PHOTORECEPTOR; PROTEIN DEFICIENCY; RETINA CONE; RETINA DEGENERATION; RETINA GANGLION CELL; RETINA ROD; TREATMENT OUTCOME; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY; VISION; ADMINISTRATION AND DOSAGE; ANIMAL; DEFICIENCY; DEPENDOPARVOVIRUS; DISEASE MODEL; GENE THERAPY; GENE VECTOR; GENETICS; HUMAN; PATHOLOGY; PATHOPHYSIOLOGY; PROCEDURES; RETINA; RETINAL DEGENERATION;

ANIMALS; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 6; DEPENDOVIRUS; DISEASE MODELS, ANIMAL; DOGS; GENETIC THERAPY; GENETIC VECTORS; HUMANS; RETINA; RETINAL DEGENERATION; RETINAL ROD PHOTORECEPTOR CELLS;

EID: 84959535401     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2016.37     Document Type: Article

References (44)

1. Sancho-Pelluz J, Arango-Gonzalez B, Kustermann S, Romero FJ, van Veen T, Zrenner E, et al. (2008). Photoreceptor cell death mechanisms in inherited retinal degeneration. Mol Neurobiol 38: 253-269.
2. Danciger M, Heilbron V, Gao YQ, Zhao DY, Jacobson SG and Farber DB (1996). A homozygous PDE6B mutation in a family with autosomal recessive retinitis pigmentosa. Mol Vis 2: 10.
3. McLaughlin ME, Sandberg MA, Berson EL and Dryja TP (1993). Recessive mutations in the gene encoding the beta-subunit of rod phosphodiesterase in patients with retinitis pigmentosa. Nat Genet 4: 130-134.
4. McLaughlin ME, Ehrhart TL, Berson EL and Dryja TP (1995). Mutation spectrum of the gene encoding the beta subunit of rod phosphodiesterase among patients with autosomal recessive retinitis pigmentosa. Proc Natl Acad Sci USA 92: 3249-3253.
5. Hartong DT, Berson EL and Dryja TP (2006). Retinitis pigmentosa. Lancet 368: 1795-1809.
6. Clark GR, Crowe P, Muszynska D, O?Prey D, O?Neill J, Alexander S, et al. (2010). Development of a diagnostic genetic test for simplex and autosomal recessive retinitis pigmentosa. Ophthalmology 117: 2169-77.e3.
7. Danciger M, Blaney J, Gao YQ, Zhao DY, Heckenlively JR, Jacobson SG, et al. (1995). Mutations in the PDE6B gene in autosomal recessive retinitis pigmentosa. Genomics 30: 1-7.
8. Collin RW, van den Born LI, Klevering BJ, de Castro-Miro M, Littink KW, Arimadyo K, et al. (2011). High-resolution homozygosity mapping is a powerful tool to detect novel mutations causative of autosomal recessive RP in the Dutch population. Invest Ophthalmol Vis Sci 52: 2227-2239.
9. Tsang SH, Tsui I, Chou CL, Zernant J, Haamer E, Iranmanesh R, et al. (2008). A novel mutation and phenotypes in phosphodiesterase 6 deficiency. Am J Ophthalmol 146: 780-788.
10. Jacobson SG, Sumaroka A, Aleman TS, Cideciyan AV, Danciger M and Farber DB (2007). Evidence for retinal remodelling in retinitis pigmentosa caused by PDE6B mutation. Br J Ophthalmol 91: 699-701.
11. Bennett J, Tanabe T, Sun D, Zeng Y, Kjeldbye H, Gouras P, et al. (1996). Photoreceptor cell rescue in retinal degeneration (rd) mice by in vivo gene therapy. Nat Med 2: 649-654.
12. Jomary C, Vincent KA, Grist J, Neal MJ and Jones SE (1997). Rescue of photoreceptor function by AAV-mediated gene transfer in a mouse model of inherited retinal degeneration. Gene Ther 4: 683-690.
13. Kumar-Singh R and Farber DB (1998). Encapsidated adenovirus mini-chromosomemediated delivery of genes to the retina: application to the rescue of photoreceptor degeneration. Hum Mol Genet 7: 1893-1900.
14. Takahashi M, Miyoshi H, Verma IM and Gage FH (1999). Rescue from photoreceptor degeneration in the rd mouse by human immunodeficiency virus vector-mediated gene transfer. J Virol 73: 7812-7816.
15. Pang JJ, Boye SL, Kumar A, Dinculescu A, Deng W, Li J, et al. (2008). AAV-mediated gene therapy for retinal degeneration in the rd10 mouse containing a recessive PDEbeta mutation. Invest Ophthalmol Vis Sci 49: 4278-4283.
16. Allocca M, Manfredi A, Iodice C, Di Vicino U and Auricchio A (2011). AAVmediated gene replacement, either alone or in combination with physical and pharmacological agents, results in partial and transient protection from photoreceptor degeneration associated with betaPDE deficiency. Invest Ophthalmol Vis Sci 52: 5713-5719.
17. Pang JJ, Dai X, Boye SE, Barone I, Boye SL, Mao S, et al. (2011). Long-term 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.
18. Nishiguchi KM, Carvalho LS, Rizzi M, Powell K, Holthaus SM, Azam SA, et al. (2015). Gene therapy restores vision in rd1 mice after removal of a confounding mutation in Gpr179. Nat Commun 6: 6006.
19. Mowat FM, Petersen-Jones SM, Williamson H, Williams DL, Luthert PJ, Ali RR, et al. (2008). Topographical characterization of cone photoreceptors and the area centralis of the canine retina. Mol Vis 14: 2518-2527.
20. Suber ML, Pittler SJ, Qin N, Wright GC, Holcombe V, Lee RH, et al. (1993). Irish setter dogs affected with rod/cone dysplasia contain a nonsense mutation in the rod cGMP phosphodiesterase beta-subunit gene. Proc Natl Acad Sci USA 90: 3968-3972.
21. Aguirre G (1978). Retinal degenerations in the dog. I. Rod dysplasia. Exp Eye Res 26: 233-253.
22. Parry HB (1953). Degenerations of the dog retina. II. Generalized progressive atrophy of hereditary origin. Br J Ophthalmol 37: 487-502.
23. Petit L, Lheriteau 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.
24. Szel A, Rohlich P, Caffe AR and van Veen T (1996). Distribution of cone photoreceptors in the mammalian retina. Microsc Res Tech 35: 445-462.
25. Szel A, Rohlich P, Mieziewska K, Aguirre G and van Veen T (1993). Spatial and temporal differences between the expression of short- and middle-wave sensitive cone pigments in the mouse retina: a developmental study. J Comp Neurol 331: 564-577.
26. Ortin-Martinez A, Jimenez-Lopez M, Nadal-Nicolas FM, Salinas-Navarro M, Alarcon-Martinez L, Sauve Y, et al. (2010). Automated quantification and topographical distribution of the whole population of S- and L-cones in adult albino and pigmented rats. Invest Ophthalmol Vis Sci 51: 3171-3183.
27. Kim C, Kim KJ, Bok J, Lee EJ, Kim DJ, Oh JH, et al. (2012). Microarray-based mutation detection and phenotypic characterization in Korean patients with retinitis pigmentosa. Mol Vis 18: 2398-2410.
28. Lin B, Masland RH and Strettoi E (2009). Remodeling of cone photoreceptor cells after rod degeneration in rd mice. Exp Eye Res 88: 589-599.
29. Milam AH, Li ZY and Fariss RN (1998). Histopathology of the human retina in retinitis pigmentosa. Prog Retin Eye Res 17: 175-205.
30. Jacobson SG, Roman AJ, Aleman TS, Sumaroka A, Herrera W, Windsor EA, et al. (2010). Normal central retinal function and structure preserved in retinitis pigmentosa. Invest Ophthalmol Vis Sci 51: 1079-1085.
31. Ait-Ali N, Fridlich R, Millet-Puel G, Clerin E, Delalande F, Jaillard C, et al. (2015). Rod-derived cone viability factor promotes cone survival by stimulating aerobic glycolysis. Cell 161: 817-832.
32. Punzo C, Kornacker K and Cepko CL (2009). Stimulation of the insulin/mTOR pathway delays cone death in a mouse model of retinitis pigmentosa. Nat Neurosci 12: 44-52.
33. Mohand-Said S, Deudon-Combe A, Hicks D, Simonutti M, Forster V, Fintz AC, et al. (1998). Normal retina releases a diffusible factor stimulating cone survival in the retinal degeneration mouse. Proc Natl Acad Sci USA 95: 8357-8362.
34. Komeima K, Rogers BS and Campochiaro PA (2007). Antioxidants slow photoreceptor cell death in mouse models of retinitis pigmentosa. J Cell Physiol 213: 809-815.
35. 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.
36. Mowat FM, Breuwer AR, Bartoe JT, Annear MJ, Zhang Z, Smith AJ, et al. (2013). RPE65 gene therapy slows cone loss in Rpe65-deficient dogs. Gene Ther 20: 545-555.
37. Acland GM, Aguirre GD, Ray J, Zhang Q, Aleman TS, Cideciyan AV, et al. (2001). Gene therapy restores vision in a canine model of childhood blindness. Nat Genet 28: 92-95.
38. Narfstrom K, Katz ML, Ford M, Redmond TM, Rakoczy E and Bragadottir R (2003). In vivo gene therapy in young and adult RPE65-/- dogs produces long-term visual improvement. J Hered 94: 31-37.
39. Rolling F, Le Meur G, Stieger K, Smith AJ, Weber M, Deschamps JY, et al. (2006). Gene therapeutic prospects in early onset of severe retinal dystrophy: restoration of vision in RPE65 Briard dogs using an AAV serotype 4 vector that specifically targets the retinal pigmented epithelium. Bull Mem Acad R Med Belg 161: 497-508; discussion 508.
40. Jacobson SG, Cideciyan AV, Roman AJ, Sumaroka A, Schwartz SB, Heon E, et al. (2015). Improvement and decline in vision with gene therapy in childhood blindness. N Engl J Med 372: 1920-1926.
41. Bainbridge JW, Mehat MS, Sundaram V, Robbie SJ, Barker SE, Ripamonti C, et al. (2015). Long-term effect of gene therapy on Leber?s congenital amaurosis. N Engl J Med 372: 1887-1897.
42. Koch SF, Tsai YT, Duong JK, Wu WH, Hsu CW, Wu WP, et al. (2015). Halting progressive neurodegeneration in advanced retinitis pigmentosa. J Clin Invest 125: 3704-3713.
43. Narfstrom K, Ekesten B, Rosolen SG, Spiess BM, Percicot CL and Ofri R; Committee for a Harmonized ERG Protocol European College of Veterinary Ophthalmology (2002). Guidelines for clinical electroretinography in the dog. Doc Ophthalmol 105: 83-92.
44. Lheriteau E, Libeau L, Mendes-Madeira A, Deschamps JY, Weber M, Le Meur G, et al. (2010). Regulation of retinal function but nonrescue of vision in RPE65-deficient dogs treated with doxycycline-regulatable AAV vectors. Mol Ther 18: 1085-1093.