Transient photoreceptor deconstruction by CNTF enhances rAAV-Mediated cone functional rescue in late stage CNGB3-achromatopsia

Molecular Therapy

Volumn 21, Issue 6, 2013, Pages 1131-1141

  Komáromy, András M ^a,b   Rowlan, Jessica S ^a   Corr, Amanda T Parton ^a   Reinstein, Shelby L ^a   Boye, Sanford L ^c   Cooper, Ann E ^a   Gonzalez, Amaliris ^d   Levy, Britt ^a   Wen, Rong ^e   Hauswirth, William W ^c,f   Beltran, William A ^a   Aguirre, Gustavo D ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

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

^d Temple University   (United States)

^e UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^f UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CILIARY NEUROTROPHIC FACTOR; CYCLIC NUCLEOTIDE GATED CHANNEL; PARVOVIRUS VECTOR; RECOMBINANT CILIARY NEUROTROPHIC FACTOR; VIRUS DNA;

ADENO ASSOCIATED VIRUS; ADENO ASSOCIATED VIRUS 5; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEDIFFERENTIATION; CNGB3 GENE; COLOR BLINDNESS; CONTROLLED STUDY; DOG; DRUG EFFICACY; FEMALE; GENE; GENE ACTIVITY; GENE FUNCTION; GENETIC TRANSDUCTION; MALE; NONHUMAN; PHOTORECEPTOR; RETINA CONE; TISSUE REGENERATION; TREATMENT OUTCOME; VIRAL GENE THERAPY; VISUAL SYSTEM FUNCTION; VISUAL SYSTEM PARAMETERS;

ADENO-ASSOCIATED VIRUS; CANIS FAMILIARIS;

EID: 84878538674     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2013.50     Document Type: Article

References (50)

1. Maguire, AM, Simonelli, F, Pierce, EA, Pugh, EN Jr, Mingozzi, F, Bennicelli, J et al. (2008). Safety and effcacy of gene transfer for Leber's congenital amaurosis. N Engl J Med 358: 2240-2248.
2. Bainbridge, JW, Smith, AJ, Barker, SS, Robbie, S, Henderson, R, Balaggan, K et al. (2008). Effect of gene therapy on visual function in Leber's congenital amaurosis. N Engl J Med 358: 2231-2239.
3. Cideciyan, AV, Aleman, TS, Boye, SL, Schwartz, SB, Kaushal, S, Roman, AJ et al. (2008). Human gene therapy for RPE65 isomerase defciency activates the retinoid cycle of vision but with slow rod kinetics. Proc Natl Acad Sci USA 105: 15112-15117.
4. Jacobson, SG, Cideciyan, AV, Ratnakaram, R, Heon, E, Schwartz, SB, Roman, AJ et al. (2012). Gene therapy for leber congenital amaurosis caused by RPE65 mutations: safety and effcacy in 15 children and adults followed up to 3 years. Arch Ophthalmol 130: 9-24.
5. Bennett, J, Ashtari, M, Wellman, J, Marshall, KA, Cyckowski, LL, Chung, DC et al. (2012). AAV2 gene therapy readministration in three adults with congenital blindness. Sci Transl Med 4: 120ra15.
6. Jacobson, SG, Acland, GM, Aguirre, GD, Aleman, TS, Schwartz, SB, Cideciyan, AV et al. (2006). Safety of recombinant adeno-associated virus type 2-RPE65 vector delivered by ocular subretinal injection. Mol Ther 13: 1074-1084.
7. Jacobson, SG, Boye, SL, Aleman, TS, Conlon, TJ, Zeiss, CJ, Roman, AJ et al. (2006). Safety in nonhuman primates of ocular AAV2-RPE65, a candidate treatment for blindness in Leber congenital amaurosis. Hum Gene Ther 17: 845-858.
8. 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.
9. Pang, JJ, Chang, B, Kumar, A, Nusinowitz, S, Noorwez, SM, Li, J et al. (2006). Gene therapy restores vision-dependent behavior as well as retinal structure and function in a mouse model of RPE65 Leber congenital amaurosis. Mol Ther 13: 565-572.
10. 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.
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. Alexander, JJ, Umino, Y, Everhart, D, Chang, B, Min, SH, Li, Q et al. (2007). Restoration of cone vision in a mouse model of achromatopsia. Nat Med 13: 685-687.
13. Michalakis, S, Mühlfriedel, R, Tanimoto, N, Krishnamoorthy, V, Koch, S, Fischer, MD et al. (2010). Restoration of cone vision in the CNGA3-/-mouse model of congenital complete lack of cone photoreceptor function. Mol Ther 18: 2057-2063.
14. Carvalho, LS, Xu, J, Pearson, RA, Smith, AJ, Bainbridge, JW, Morris, LM et al. (2011). Long-term and age-dependent restoration of visual function in a mouse model of CNGB3-associated achromatopsia following gene therapy. Hum Mol Genet 20: 3161-3175.
15. Pang, JJ, Deng, WT, Dai, X, Lei, B, Everhart, D, Umino, Y et al. (2012). AAV-mediated cone rescue in a naturally occurring mouse model of CNGA3-achromatopsia. PLoS ONE 7: e35250.
16. 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.
17. 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.
18. 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.
19. 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.
20. Ali, RR, Sarra, GM, Stephens, C, Alwis, MD, Bainbridge, JW, Munro, PM et al. (2000). Restoration of photoreceptor ultrastructure and function in retinal degeneration slow mice by gene therapy. Nat Genet 25: 306-310.
21. Sarra, GM, Stephens, C, de Alwis, M, Bainbridge, JW, Smith, AJ, Thrasher, AJ et al. (2001). Gene replacement therapy in the retinal degeneration slow (rds) mouse: the effect on retinal degeneration following partial transduction of the retina. Hum Mol Genet 10: 2353-2361.
22. Pang, J, Boye, SE, Lei, B, Boye, SL, Everhart, D, Ryals, R et al. (2010). Self-complementary AAV-mediated gene therapy restores cone function and prevents cone degeneration in two models of Rpe65 defciency. Gene Ther 17: 815-826.
23. Kong, F, Li, W, Li, X, Zheng, Q, Dai, X, Zhou, X et al. (2010). Self-complementary AAV5 vector facilitates quicker transgene expression in photoreceptor and retinal pigment epithelial cells of normal mouse. Exp Eye Res 90: 546-554.
24. Petrs-Silva, H, Dinculescu, A, Li, Q, Min, SH, Chiodo, V, Pang, JJ et al. (2009). High-effciency transduction of the mouse retina by tyrosine-mutant AAV serotype vectors. Mol Ther 17: 463-471.
25. Kohl, S, Varsanyi, B, Antunes, GA, Baumann, B, Hoyng, CB, Jägle, H et al. (2005). CNGB3 mutations account for 50% of all cases with autosomal recessive achromatopsia. Eur J Hum Genet 13: 302-308.
26. Sundin, OH, Yang, JM, Li, Y, Zhu, D, Hurd, JN, Mitchell, TN et al. (2000). Genetic basis of total colourblindness among the Pingelapese islanders. Nat Genet 25: 289-293.
27. Sidjanin, DJ, Lowe, JK, McElwee, JL, Milne, BS, Phippen, TM, Sargan, DR et al. (2002). Canine CNGB3 mutations establish cone degeneration as orthologous to the human achromatopsia locus ACHM3. Hum Mol Genet 11: 1823-1833.
28. Ding, XQ, Harry, CS, Umino, Y, Matveev, AV, Fliesler, SJ and Barlow, RB (2009). Impaired cone function and cone degeneration resulting from CNGB3 defciency: down-regulation of CNGA3 biosynthesis as a potential mechanism. Hum Mol Genet 18: 4770-4780.
29. Wen, R, Tao, W, Li, Y and Sieving, PA (2012). CNTF and retina. Prog Retin Eye Res 31: 136-151.
30. Wen, R, Song, Y, Kjellstrom, S, Tanikawa, A, Liu, Y, Li, Y et al. (2006). Regulation of rod phototransduction machinery by ciliary neurotrophic factor. J Neurosci 26: 13523-13530.
31. Fisher, SK, Lewis, GP, Linberg, KA and Verardo, MR (2005). Cellular remodeling in mammalian retina: results from studies of experimental retinal detachment. Prog Retin Eye Res 24: 395-431.
32. Beltran, WA, Wen, R, Acland, GM and Aguirre, GD (2007). Intravitreal injection of ciliary neurotrophic factor (CNTF) causes peripheral remodeling and does not prevent photoreceptor loss in canine RPGR mutant retina. Exp Eye Res 84: 753-771.
33. Li, Y, Tao, W, Luo, L, Huang, D, Kauper, K, Stabila, P et al. (2010). CNTF induces regeneration of cone outer segments in a rat model of retinal degeneration. PLoS ONE 5: e9495.
34. 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.
35. Gropp, KE, Szél, A, Huang, JC, Acland, GM, Farber, DB and Aguirre, GD (1996). Selective absence of cone outer segment beta 3-transducin immunoreactivity in hereditary cone degeneration (cd). Exp Eye Res 63: 285-296.
36. Komáromy, AM, Alexander, JJ, Cooper, AE, Chiodo, VA, Glushakova, LG, Acland, GM et al. (2008). Targeting gene expression to cones with human cone opsin promoters in recombinant AAV. Gene Ther 15: 1049-1055.
37. Akhmedov, NB, Piriev, NI, Pearce-Kelling, S, Acland, GM, Aguirre, GD and Farber, DB (1998). Canine cone transducin-gamma gene and cone degeneration in the cd dog. Invest Ophthalmol Vis Sci 39: 1775-1781.
38. Berta, ÁI, Boesze-Battaglia, K, Genini, S, Goldstein, O, O'Brien, PJ, Szél, Á et al. (2011). Photoreceptor cell death, proliferation and formation of hybrid rod/S-cone photoreceptors in the degenerating STK38L mutant retina. PLoS ONE 6: e24074.
39. Beltran, WA, Hammond, P, Acland, GM and Aguirre, GD (2006). A frameshift mutation in RPGR exon ORF15 causes photoreceptor degeneration and inner retina remodeling in a model of X-linked retinitis pigmentosa. Invest Ophthalmol Vis Sci 47: 1669-1681.
40. Beltran, WA, Rohrer, H and Aguirre, GD (2005). Immunolocalization of ciliary neurotrophic factor receptor alpha (CNTFRalpha) in mammalian photoreceptor cells. Mol Vis 11: 232-244.
41. Acland, GM and Aguirre, GD (1987). Retinal degenerations in the dog: IV. Early retinal degeneration (erd) in Norwegian elkhounds. Exp Eye Res 44: 491-521.
42. Matulef, K and Zagotta, WN (2003). Cyclic nucleotide-gated ion channels. Annu Rev Cell Dev Biol 19: 23-44.
43. Thapa, A, Morris, L, Xu, J, Ma, H, Michalakis, S, Biel, M et al. (2012). Endoplasmic reticulum stress-associated cone photoreceptor degeneration in cyclic nucleotide-gated channel defciency. J Biol Chem 287: 18018-18029.
44. Curcio, CA, Allen, KA, Sloan, KR, Lerea, CL, Hurley, JB, Klock, IB et al. (1991). Distribution and morphology of human cone photoreceptors stained with anti-blue opsin. J Comp Neurol 312: 610-624.
45. Kohl, S, Marx, T, Giddings, I, Jägle, H, Jacobson, SG, Apfelstedt-Sylla, E et al. (1998). Total colourblindness is caused by mutations in the gene encoding the alpha-subunit of the cone photoreceptor cGMP-gated cation channel. Nat Genet 19: 257-259.
46. Genead, MA, Fishman, GA, Rha, J, Dubis, AM, Bonci, DM, Dubra, A et al. (2011). Photoreceptor structure and function in patients with congenital achromatopsia. Invest Ophthalmol Vis Sci 52: 7298-7308.
47. Buch, PK, MacLaren, RE, Durán, Y, Balaggan, KS, MacNeil, A, Schlichtenbrede, FC et al. (2006). In contrast to AAV-mediated Cntf expression, AAV-mediated Gdnf expression enhances gene replacement therapy in rodent models of retinal degeneration. Mol Ther 14: 700-709.
48. Tao, W, Wen, R, Goddard, MB, Sherman, SD, O'Rourke, PJ, Stabila, PF et al. (2002). Encapsulated cell-based delivery of CNTF reduces photoreceptor degeneration in animal models of retinitis pigmentosa. Invest Ophthalmol Vis Sci 43: 3292-3298.
49. Beltran, WA, Boye, SL, Boye, SE, Chiodo, VA, Lewin, AS, Hauswirth, WW et al. (2010). rAAV2/5 gene-targeting to rods:dose-dependent effciency and complications associated with different promoters. Gene Ther 17: 1162-1174.
50. Buyukmihci, N and Aguirre, GD (1976). Rod disc turnover in the dog. Invest Ophthalmol 15: 579-584.