Drug and gene therapy of hereditary retinal disease in dog and cat models

Drug Discovery Today: Disease Models

Volumn 10, Issue 4, 2013, Pages e215-e223

  Petersen Jones, Simon M ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GUANOSINE TRIPHOSPHATASE; PHOSPHODIESTERASE VI; RHODOPSIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; CANINE MODEL; COLOR BLINDNESS; CONE ROD DYSTROPHY; FELINE MODEL; GENE MUTATION; GENE THERAPY; HUMAN; LEBER CONGENITAL AMAUROSIS; MEDICAL TERMINOLOGY; MUTANT CAT; MUTANT DOG; NONHUMAN; RETINA DYSTROPHY; RETINITIS PIGMENTOSA; RETINOPATHY; REVIEW; VITELLIFORM MACULAR DEGENERATION;

EID: 84904525999     PISSN: None     EISSN: 17406757     Source Type: Journal    
DOI: 10.1016/j.ddmod.2014.01.002     Document Type: Review

References (60)

1. [1] Gearhart, P.M., Gearhart, C.C., Petersen-Jones, S.M., A novel method for objective vision testing in canine models of inherited retinal disease. Invest Ophthalmol Vis Sci 49 (2008), 3568–3576.
2. [2] Annear, M.J., Gornik, K.R., Venturi, F.L., Hauptman, J.G., Bartoe, J.T., Petersen-Jones, S.M., Reproducibility of an objective four-choice canine vision testing technique that assesses vision at differing light intensities. Vet Ophthalmol 16 (2013), 324–328.
3. [3] Garcia, M.M., Ying, G.S., Cocores, C.A., Tanaka, J.C., Komaromy, A.M., Evaluation of a behavioral method for objective vision testing and identification of achromatopsia in dogs. Am J Vet Res 71 (2010), 97–102.
4. [4] Veske, A., Nilsson, S.E., Narfström, K., Gal, A., Retinal dystrophy of swedish Briard/Briard-beagle dogs is due to a 4-bp deletion in RPE65. Genomics 57 (1999), 57–61.
5. [5] Moiseyev, G., Chen, Y., Takahashi, Y., Wu, B.X., Ma, J.X., RPE65 is the isomerohydrolase in the retinoid visual cycle. Proc Natl Acad Sci U S A 102 (2005), 12413–12418.
6. [6] Gu, S.M., Thompson, D.A., Srikumari, C.R., Lorenz, B., Finckh, U., Nicoletti, A., et al. Mutations in RPE65 cause autosomal recessive childhood-onset severe retinal dystrophy. Nat Genet 17 (1997), 194–197.
7. [7] Acland, G.M., Aguirre, G.D., Ray, J., Zhang, Q., Aleman, T.S., Cideciyan, A.V., et al. Gene therapy restores vision in a canine model of childhood blindness. Nat Genet 28 (2001), 92–95.
8. [8] Narfström, K., Katz, M.L., Bragadottir, R., Seeliger, M., Boulanger, A., Redmond, T.M., et al. Functional and structural recovery of the retina after gene therapy in the RPE65 null mutation dog. Invest Ophthalmol Vis Sci 44 (2003), 1663–1672.
9. [9] Le Meur, G., Stieger, K., Smith, A.J., Weber, M., Deschamps, J.Y., Nivard, D., et al. Restoration of vision in RPE65-deficient Briard dogs using an AAV serotype 4 vector that specifically targets the retinal pigmented epithelium. Gene Ther. 14 (2007), 292–303.
10. [10] Bainbridge, J.W., Smith, A.J., Barker, S.S., Robbie, S., Henderson, R., Balaggan, K., et al. Effect of gene therapy on visual function in Leber's congenital amaurosis. N. Engl. J. Med. 358 (2008), 2231–2239.
11. [11] Maguire, A.M., Simonelli, F., Pierce, E.A., Pugh, E.N. Jr., Mingozzi, F., Bennicelli, J., et al. Safety and efficacy of gene transfer for Leber's congenital amaurosis. N. Engl. J. Med. 358 (2008), 2240–2248.
12. [12] Cideciyan, A.V., Aleman, T.S., Boye, S.L., Schwartz, S.B., Kaushal, S., Roman, A.J., et al. Human gene therapy for RPE65 isomerase deficiency activates the retinoid cycle of vision but with slow rod kinetics. Proc. Natl. Acad. Sci. U. S. A 105 (2008), 15112–15117.
13. [13] Annear, M.J., Bartoe, J.T., Barker, S.E., Smith, A.J., Curran, P.G., Bainbridge, J.W., et al. Gene therapy in the second eye of RPE65-deficient dogs improves retinal function. Gene Ther 18 (2011), 53–61.
14. [14] Mowat, F.M., Breuwer, A.R., Bartoe, J.T., Annear, M.J., Zhang, Z., Smith, A.J., et al. RPE65 gene therapy slows cone loss in Rpe65-deficient dogs. Gene Ther 20 (2013), 545–555.
15. [15] Cideciyan, A.V., Jacobson, S.G., Beltran, W.A., Sumaroka, A., Swider, M., Iwabe, S., et al. Human retinal gene therapy for Leber congenital amaurosis shows advancing retinal degeneration despite enduring visual improvement. Proc Natl Acad Sci U S A 110 (2013), E517–E525.
16. [16] Gearhart, P.M., Gearhart, C., Thompson, D.A., Petersen-Jones, S.M., Improvement of visual performance with intravitreal administration of 9-cis-retinal in Rpe65-mutant dogs. Arch Ophthalmol 128 (2010), 1442–1448.
17. [17] Van Hooser, J.P., Aleman, T.S., He, Y.G., Cideciyan, A.V., Kuksa, V., Pittler, S.J., et al. Rapid restoration of visual pigment and function with oral retinoid in a mouse model of childhood blindness. Proc Natl Acad Sci U S A 97 (2000), 8623–8628.
18. [18] Menotti-Raymond, M., David, V.A., Schaffer, A.A., Stephens, R., Wells, D., Kumar-Singh, R., et al. Mutation in CEP290 discovered for cat model of human retinal degeneration. J Hered 98 (2007), 211–220.
19. [19] Coppieters, F., Lefever, S., Leroy, B.P., De Baere, E., CEP290, a gene with many faces: mutation overview and presentation of CEP290base. Hum Mutat 31 (2010), 1097–1108.
20. [20] Rachel, R.A., Li, T., Swaroop, A., Photoreceptor sensory cilia and ciliopathies: focus on CEP290, RPGR and their interacting proteins. Cilia, 1, 2012, 22.
21. [21] Seiler, M.J., Aramant, R.B., Seeliger, M.W., Bragadottir, R., Mahoney, M., Narfström, K., Functional and structural assessment of retinal sheet allograft transplantation in feline hereditary retinal degeneration. Vet Ophthalmol 12 (2009), 158–169.
22. [22] Klassen, H., Schwartz, P.H., Ziaeian, B., Nethercott, H., Young, M.J., Bragadottir, R., et al. Neural precursors isolated from the developing cat brain show retinal integration following transplantation to the retina of the dystrophic cat. Vet Ophthalmol 10 (2007), 245–253.
23. [23] Chong, N.H., Alexander, R.A., Waters, L., Barnett, K.C., Bird, A.C., Luthert, P.J., Repeated injections of a ciliary neurotrophic factor analogue leading to long-term photoreceptor survival in hereditary retinal degeneration. Invest Ophthalmol Vis Sci 40 (1999), 1298–1305.
24. [24] Suber, M.L., Pittler, S.J., Quin, N., Wright, G.C., Holcombe, N., Lee, R.H., et al. Irish setter dogs affected with rod-cone dysplasia contain a nonsense mutation in the rod cGMP phosphodiesterase beta-subunit gene. Proc Natl Acad Sci U S A 90 (1993), 3968–3972.
25. [25] Petersen-Jones, S.M., Entz, D.D., Sargan, D.R., cGMP phosphodiesterase-α mutation causes progressive retinal atrophy in the Cardigan Welsh corgi dog. Invest Ophthalmol Vis Sci 40 (1999), 1637–1644.
26. [26] Tuntivanich, N., Pittler, S.J., Fischer, A.J., Omar, G., Kiupel, M., Weber, A.J., et al. Characterization of a canine model of autosomal recessive retinitis pigmentosa due to a PDE6A mutation. Invest Ophthalmol Vis Sci 50 (2009), 801–813.
27. [27] Tao, W., Wen, R., Goddard, M.B., Sherman, S.D., O'Rourke, P.J., Stabila, P.F., et al. Encapsulated cell-based delivery of CNTF reduces photoreceptor degeneration in animal models of retinitis pigmentosa. Invest Ophthalmol Vis Sci 43 (2002), 3292–3298.
28. [28] Sieving, P.A., Caruso, R.C., Tao, W., Coleman, H.R., Thompson, D.J., Fullmer, K.R., et al. Ciliary neurotrophic factor (CNTF) for human retinal degeneration: phase I trial of CNTF delivered by encapsulated cell intraocular implants. Proc Natl Acad Sci U S A 103 (2006), 3896–3901.
29. [29] Petit, L., Lheriteau, E., Weber, M., Le Meur, G., Deschamps, J.Y., Provost, N., et al. Restoration of vision in the pde6beta-deficient dog, a large animal model of rod-cone dystrophy. Mol Ther 20 (2012), 2019–2030.
30. [30] Mowat, F.M., Bartoe, J.T., Bruewer, A., Dinculescu, A., Boye, S.L., Hauswirth, W.W., et al. Evaluation Of Rod Photoreceptor Function And Preservation Following Retinal Gene Therapy In The PDE6A Mutant Dog. ARVO Meeting Abstracts, 53, 2012, 1928.
31. [31] Kijas, J.W., Cideciyan, A.V., Aleman, T.S., Pianta, M.J., Pearce-Kelling, S.E., Miller, B.J., et al. Naturally occurring rhodopsin mutation in the dog causes retinal dysfunction and degeneration mimicking human dominant retinitis pigmentosa. Proc Natl Acad Sci U S A 99 (2002), 6328–6333.
32. [32] Cideciyan, A.V., Jacobson, S.G., Aleman, T.S., Gu, D., Pearce-Kelling, S.E., Sumaroka, A., et al. In vivo dynamics of retinal injury and repair in the rhodopsin mutant dog model of human retinitis pigmentosa. Proc Natl Acad Sci U S A 102 (2005), 5233–5238.
33. [33] Gu, D., Beltran, W.A., Pearce-Kelling, S., Li, Z., Acland, G.M., Aguirre, G.D., Steroids do not prevent photoreceptor degeneration in the light-exposed T4R rhodopsin mutant dog retina irrespective of AP-i inhibition. Invest Ophthalmol Vis Sci 50 (2009), 3482–3494.
34. [34] Hosch, J., Lorenz, B., Stieger, K., RPGR: role in the photoreceptor cilium, human retinal disease, and gene therapy. Ophthalmic Genet 32 (2011), 1–11.
35. [35] Sidjanin, D.J., Lowe, J.K., McElwee, J.L., Milne, B.S., Phippen, T.M., Sargan, D.R., et al. Canine CNGB3 mutations establish cone degeneration as orthologous to the human achromatopsia locus ACHM3. Hum Mol Genet 11 (2002), 1823–1833.
36. [36] Komaromy, A.M., Alexander, J.J., Rowlan, J.S., Garcia, M.M., Chiodo, V.A., Kaya, A., et al. Gene therapy rescues cone function in congenital achromatopsia. Hum Mol Genet 19 (2010), 2581–2593.
37. [37] Wen, R., Tao, W., Li, Y., Sieving, P.A., CNTF and retina. Prog Retin Eye Res 31 (2012), 136–151.
38. [38] Grahn, B.H., Cullen, C.L., Retinopathy of Great Pyrenees dogs: fluorescein angiography, light microscopy and transmitting and scanning electron microscopy. Vet Ophthalmol 4 (2001), 191–199.
39. [39] Guziewicz, K.E., Zangerl, B., Lindauer, S.J., Mullins, R.F., Sandmeyer, L.S., Grahn, B.H., et al. Bestrophin gene mutations cause canine multifocal retinopathy: a novel animal model for best disease. Invest Ophthalmol Vis Sci 48 (2007), 1959–1967.
40. [40] Hartzell, H.C., Qu, Z., Yu, K., Xiao, Q., Chien, L.T., Molecular physiology of bestrophins: multifunctional membrane proteins linked to best disease and other retinopathies. Physiol Rev 88 (2008), 639–672.
41. [41] Zangerl, B., Wickstrom, K., Slavik, J., Lindauer, S.J., Ahonen, S., Schelling, C., et al. Assessment of canine BEST1 variations identifies new mutations and establishes an independent bestrophinopathy model (cmr3). Mol Vis 16 (2010), 2791–2804.
42. [42] Guziewicz, K.E., Slavik, J., Lindauer, S.J., Aguirre, G.D., Zangerl, B., Molecular consequences of BEST1 gene mutations in canine multifocal retinopathy predict functional implications for human bestrophinopathies. Invest Ophthalmol Vis Sci 52 (2011), 4497–4505.
43. [43] Rossmiller, B., Mao, H., Lewin, A.S., Gene therapy in animal models of autosomal dominant retinitis pigmentosa. Mol Vis 18 (2012), 2479–2496.
44. [44] Bartoe, J.T., Mowat, F., Dinculescu, A., Boye, S., Hauswirth, W., Petersen-Jones, S., AAV Vectors With Engineered Capsid Mutations Efficiently Transduce Outer Retina With Intravitreal Delivery And Result In Rapid Gene Expression With Subretinal Delivery In Dogs. ARVO Meeting Abstracts, 52, 2011, 1420.
45. [45] Charman, W.N., Optics of the human eye. Cronly, D.J., (eds.) Visual optics and instrumentation, 1991, CRC Press, 1–26.
46. [46] Tuntivanich, N., Petersen-Jones, S.M., Steibel, J.P., Johnson, C., Forcier, J.Q., Postnatal development of canine axial globe length measured by B-scan ultrasonography. Vet Ophthalmol 10 (2007), 2–5.
47. [47] Schiffer, S.P., Rantanen, N.W., Leary, G.A., Bryan, G.M., Biometric study of the canine eye, using A-mode ultrasonography. Am J Vet Res 43 (1982), 826–830.
48. [48] Schippert, R., Burkhardt, E., Feldkaemper, M., Schaeffel, F., Relative axial myopia in Egr-1 (ZENK) knockout mice. Invest Ophthalmol Vis Sci 48 (2007), 11–17.
49. [49] Menotti-Raymond, M., Deckman, K.H., David, V., Myrkalo, J., O'Brien, S.J., Narfström, K., Mutation discovered in a feline model of human congenital retinal blinding disease. Invest Ophthalmol Vis. Sci. 51 (2010), 2852–2859.
50. [50] Dekomien, G., Runte, M., Godde, R., Epplen, J.T., Generalized progressive retinal atrophy of Sloughi dogs is due to an 8-bp insertion in exon 21 of the PDE6B gene. Cytogenet Cell Genet 90 (2000), 261–267.
51. [51] Kukekova, A.V., Goldstein, O., Johnson, J.L., Richardson, M.A., Pearce-Kelling, S.E., Swaroop, A., et al. Canine RD3 mutation establishes rod-cone dysplasia type 2 (rcd2) as ortholog of human and murine rd3. Mamm Genome 20 (2009), 109–123.
52. [52] Winkler, P.A., Ekenstedt, K.J., Occelli, L.M., Frattaroli, A.V., Bartoe, J.T., Venta, P.J., et al. A large animal model for CNGB1 autosomal recessive retinitis pigmentosa. PLoS ONE, 8, 2013, e72229.
53. [53] Zangerl, B., Goldstein, O., Lindauer, S.J.P., Pearce-Kelling, S.E., Philp, A.R., Antosh, A., et al. Novel Retinal Gene (PRCD) Causes Progressive Rod-Cone Degeneration in Canines and Humans. Invest Ophthalmol Vis Sci, 47, 2006, 2972.
54. [54] Downs, L.M., Wallin-Hakansson, B., Boursnell, M., Marklund, S., Hedhammar, A., Truve, K., et al. A frameshift mutation in golden retriever dogs with progressive retinal atrophy endorses SLC4A3 as a candidate gene for human retinal degenerations. PLoS One, 6, 2011, e21452.
55. [55] Goldstein, O., Kukekova, A.V., Aguirre, G.D., Acland, G.M., Exonic SINE insertion in STK38L causes canine early retinal degeneration (erd). Genomics 96 (2010), 362–368.
56. [56] Downs, L.M., Bell, J.S., Freeman, J., Hartley, C., Hayward, L.J., Mellersh, C.S., Late-onset progressive retinal atrophy in the Gordon and Irish Setter breeds is associated with a frameshift mutation in C2orf71. Anim Genet 44 (2012), 169–177.
57. [57] Zhang, Q., Acland, G.M., Wu, W.X., Johnson, J.L., Pearce-Kelling, S., Tulloch, B., et al. Different RPGR exon ORF15 mutations in Canids provide insights into photoreceptor cell degeneration. Hum Mol Genet 11 (2002), 993–1003.
58. [58] Wiik, A.C., Wade, C., Biagi, T., Ropstad, E.O., Bjerkas, E., Lindblad-Toh, K., et al. A deletion in nephronophthisis 4 (NPHP4) is associated with recessive cone-rod dystrophy in standard wire-haired dachshund. Genome Res 18 (2008), 1415–1421.
59. [59] Goldstein, O., Mezey, J.G., Boyko, A.R., Gao, C., Wang, W., Bustamante, C.D., et al. An ADAM9 mutation in canine cone-rod dystrophy 3 establishes homology with human cone-rod dystrophy 9. Mol Vis 16 (2010), 1549–1569.
60. [60] Kropatsch, R., Petrasch-Parwez, E., Seelow, D., Schlichting, A., Gerding, W.M., Akkad, D.A., et al. Generalized progressive retinal atrophy in the Irish Glen of Imaal Terrier is associated with a deletion in the ADAM9 gene. Mol Cell Probes 24 (2010), 357–363.