Gene therapy restores vision and delays degeneration in the CNGB1-/- mouse model of retinitis pigmentosa

Human Molecular Genetics

Volumn 21, Issue 20, 2012, Pages 4486-4496

  Koch, Susanne ^a   Sothilingam, Vithiyanjali ^b   Garcia garrido, Marina ^b   Tanimoto, Naoyuki ^b   Becirovic, Elvir ^a   Koch, Fred ^a   Seide, Christina ^b   Beck, Susanne C ^b   Seeliger, Mathias W ^b   Biel, Martin ^a   Mühlfriedel, Regine ^b   Michalakis, Stylianos ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; COMPLEMENTARY DNA; CYCLIC NUCLEOTIDE GATED CHANNEL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLINDNESS; CHANNELOPATHY; CNGB1A GENE; ELECTRORETINOGRAPHY; GENE; GENE MUTATION; GENE REPLACEMENT THERAPY; GENE THERAPY; HUMAN; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RETINA DEGENERATION; RETINA ROD; RETINA ROD OUTER SEGMENT; RETINITIS PIGMENTOSA; VISION; VISUAL SYSTEM;

ANIMALS; CYCLIC NUCLEOTIDE-GATED CATION CHANNELS; DEPENDOVIRUS; DISEASE MODELS, ANIMAL; DNA, COMPLEMENTARY; ELECTRORETINOGRAPHY; GENETIC THERAPY; GENETIC VECTORS; MICE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; RETINAL DEGENERATION; RETINITIS PIGMENTOSA; RHODOPSIN; ROD CELL OUTER SEGMENT;

MUS;

EID: 84867122079     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/dds290     Document Type: Article

References (39)

1. Hartong, D.T., Berson, E.L. and Dryja, T.P. (2006) Retinitis pigmentosa. Lancet, 368, 1795-1809.
2. Sahel, J., Bonnel, S., Mrejen, S. and Paques, M. (2010) Retinitis pigmentosa and other dystrophies. Dev. Ophthalmol., 47, 160-167.
3. Cideciyan, A.V. (2010) Leber congenital amaurosis due to RPE65 mutations and its treatment with gene therapy. Prog. Retin. Eye Res., 29, 398-427.
4. Biel, M. and Michalakis, S. (2007) Function and dysfunction of CNG channels: insights from channelopathies and mouse models. Mol. Neurobiol., 35, 266-277.
5. Biel, M. and Michalakis, S. (2009) Cyclic nucleotide-gated channels. Handb. Exp. Pharmacol., 191, 111-136.
6. Hüttl, S., Michalakis, S., Seeliger, M., Luo, D.G., Acar, N., Geiger, H., Hudl, K., Mader, R., Haverkamp, S., Moser, M. et al. (2005) Impaired channel targeting and retinal degeneration in mice lacking the cyclic nucleotide-gated channel subunit CNGB1. J. Neurosci., 25, 130-138.
7. Zhang, Y., Molday, L.L., Molday, R.S., Sarfare, S.S., Woodruff, M.L., Fain, G.L., Kraft, T.W. and Pittler, S.J. (2009) Knockout of GARPs and the beta-subunit of the rod cGMP-gated channel disrupts disk morphogenesis and rod outer segment structural integrity. J. Cell Sci., 122, 1192-1200.
8. Wu, Z.J., Yang, H.Y. and Colosi, P. (2010) Effect of genome size on AAV vector packaging. Mol. Ther., 18, 80-86.
9. Lai, Y., Yue, Y.P. and Duan, D.S. (2010) Evidence for the failure of adeno-associated virus serotype 5 to package a viral genome ≥8.2 kb. Mol. Ther., 18, 75-79.
10. Dong, B.A., Nakai, H. and Xiao, W.D. (2010) Characterization of genome integrity for oversized recombinant AAV vector. Mol. Ther., 18, 87-92.
11. Flannery, J.G., Zolotukhin, S., Vaquero, M.I., LaVail, M.M., Muzyczka, N. and Hauswirth, W.W. (1997) Efficient photoreceptor-targeted gene expression in vivo by recombinant adeno-associated virus. Proc. Natl Acad. Sci. USA, 94, 6916-6921.
12. Petrs-Silva, H., Dinculescu, A., Li, Q., Min, S.H., Chiodo, V., Pang, J.J., Zhong, L., Zolotukhin, S., Srivastava, A., Lewin, A.S. et al. (2009) High-efficiency transduction of the mouse retina by tyrosine-mutant AAV serotype vectors. Mol. Ther., 17, 463-471.
13. Seeliger, M.W., Beck, S.C., Pereyra-Munoz, N., Dangel, S., Tsai, J.Y., Luhmann, U.F., van de Pavert, S.A., Wijnholds, J., Samardzija, M., Wenzel, A. et al. (2005) In vivo confocal imaging of the retina in animal models using scanning laser ophthalmoscopy. Vision Res., 45, 3512-3519.
14. Fischer, M.D., Huber, G., Beck, S.C., Tanimoto, N., Muehlfriedel, R., Fahl, E., Grimm, C., Wenzel, A., Reme, C.E., van de Pavert, S.A. et al. (2009) Noninvasive, in vivo assessment of mouse retinal structure using optical coherence tomography. PLoS ONE, 4, e7507.
15. Spaide, R.F. and Curcio, C.A. (2011) Anatomical correlates to the bands seen in the outer retina by optical coherence tomography: literature review and model. Retina, 31, 1609-1619.
16. Michalakis, S., Geiger, H., Haverkamp, S., Hofmann, F., Gerstner, A. and Biel, M. (2005) Impaired opsin targeting and cone photoreceptor migration in the retina of mice lacking the cyclic nucleotide-gated channel CNGA3. Invest. Ophthalmol. Vis. Sci., 46, 1516-1524.
17. den Hollander, A.I., Black, A., Bennett, J. and Cremers, F.P. (2010) Lighting a candle in the dark: advances in genetics and gene therapy of recessive retinal dystrophies. J. Clin. Invest., 120, 3042-3053.
18. Smith, A.J., Bainbridge, J.W. and Ali, R.R. (2012) Gene supplementation therapy for recessive forms of inherited retinal dystrophies. Gene Ther., 19, 154-161.
19. 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. Engl. J. Med., 358, 2231-2239.
20. 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. USA, 105, 15112-15117.
21. Hauswirth, W.W., Aleman, T.S., Kaushal, S., Cideciyan, A.V., Schwartz, S.B., Wang, L., Conlon, T.J., Boye, S.L., Flotte, T.R., Byrne, B.J. et al. (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. Hum. Gene Ther., 19, 979-990.
22. Bennett, J., Tanabe, T., Sun, D., Zeng, Y., Kjeldbye, H., Gouras, P. and Maguire, A.M. (1996) Photoreceptor cell rescue in retinal degeneration (RD) mice by in vivo gene therapy. Nat. Med., 2, 649-654.
23. Jomary, C., Vincent, K.A., Grist, J., Neal, M.J. and Jones, S.E. (1997) Rescue of photoreceptor function by AAV-mediated gene transfer in a mouse model of inherited retinal degeneration. Gene Ther., 4, 683-690.
24. Pang, J.J., Boye, S.L., Kumar, A., Dinculescu, A., Deng, W., Li, J., Li, Q., Rani, A., Foster, T.C., Chang, B. 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.
25. Pang, J.J., Dai, X., Boye, S.E., Barone, I., Boye, S.L., Mao, S., Everhart, D., Dinculescu, A., Liu, L., Umino, Y. 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.
26. Luo, D.G., Xue, T. and Yau, K.W. (2008) How vision begins: an odyssey. Proc. Natl Acad. Sci. USA, 105, 9855-9862.
27. - mouse model of congenital complete lack of cone photoreceptor function. Mol. Ther., 18, 2057-2063.
28. Gao, G.P., Alvira, M.R., Wang, L., Calcedo, R., Johnston, J. and Wilson, J.M. (2002) Novel adeno-associated viruses from rhesus monkeys as vectors for human gene therapy. Proc. Natl Acad. Sci. USA, 99, 11854-11859.
29. Auricchio, A., Hildinger, M., O'Connor, E., Gao, G.P. and Wilson, J.M. (2001) Isolation of highly infectious and pure adeno-associated virus type 2 vectors with a single-step gravity-flow column. Hum. Gene Ther., 12, 71-76.
30. Grieger, J.C., Choi, V.W. and Samulski, R.J. (2006) Production and characterization of adeno-associated viral vectors. Nat. Protoc., 1, 1412-1428.
31. Seeliger, M.W., Grimm, C., Stahlberg, F., Friedburg, C., Jaissle, G., Zrenner, E., Guo, H., Reme, C.E., Humphries, P., Hofmann, F. et al. (2001) New views on RPE65 deficiency: the rod system is the source of vision in a mouse model of Leber congenital amaurosis. Nat. Genet., 29, 70-74.
32. Tanimoto, N., Muehlfriedel, R.L., Fischer, M.D., Fahl, E., Humphries, P., Biel, M. and Seeliger, M.W. (2009) Vision tests in the mouse: functional phenotyping with electroretinography. Front Biosci., 14, 2730-2737.
33. Molday, R.S., Molday, L.L., Dose, A., Clark-Lewis, I., Illing, M., Cook, N.J., Eismann, E. and Kaupp, U.B. (1991) The cGMP-gated channel of the rod photoreceptor cell characterization and orientation of the amino terminus. J. Biol. Chem., 266, 21917-21922.
34. Connell, G., Bascom, R., Molday, L., Reid, D., McInnes, R.R. and Molday, R.S. (1991) Photoreceptor peripherin is the normal product of the gene responsible for retinal degeneration in the rds mouse. Proc. Natl Acad. Sci. USA, 88, 723-726.
35. Tanaka, J., Markerink-van Ittersum, M., Steinbusch, H.W. and De Vente, J. (1997) Nitric oxide-mediated cGMP synthesis in oligodendrocytes in the developing rat brain. Glia, 19, 286-297.
36. Zhang, T., Baehr, W. and Fu, Y. (2012) Chemical chaperone TUDCA preserves cone photoreceptors in a mouse model of Leber congenital amaurosis. Invest. Ophthalmol. Vis. Sci., 53, 3349-3356.
37. Poetsch, A., Molday, L.L. and Molday, R.S. (2001) The cGMP-gated channel and related glutamic acid-rich proteins interact with peripherin-2 at the rim region of rod photoreceptor disc membranes. J. Biol. Chem., 276, 48009-48016.
38. Morris, R. (1984) Developments of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Methods, 11, 47-60.
39. Pang, J.J., Chang, B., Kumar, A., Nusinowitz, S., Noorwez, S.M., Li, J., Rani, A., Foster, T.C., Chiodo, V.A., Doyle, T. 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.