Safety in nonhuman primates of ocular AAV2-RPE65, a candidate treatment for blindness in Leber congenital amaurosis

Human Gene Therapy

Volumn 17, Issue 8, 2006, Pages 845-858

  Jacobson, Samuel G ^a   Boye, Sanford L ^b   Aleman, Tomas S ^a   Conlon, Thomas J ^b   Zeiss, Caroline J ^c   Roman, Alejandro J ^a   Cideciyan, Artur V ^a   Schwartz, Sharon B ^a   Komaromy, Andras M ^d   Doobrajh, Michelle ^a   Cheung, Andy Y ^a   Sumaroka, Alexander ^a   Pearce Kelling, Susan E ^e   Aguirre, Gustavo D ^d   Kaushal, Shalesh ^b   Maguire, Albert M ^a   Flotte, Terence R ^b   Hauswirth, William W ^b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

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

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

^e Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENE PRODUCT; PROTEIN AAV RPE65; UNCLASSIFIED DRUG; CARRIER PROTEIN; EYE PROTEIN; RPE65 PROTEIN, BOS TAURUS; RPE65 PROTEIN, HUMAN;

ABSENCE OF SIDE EFFECTS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLINDNESS; CONTROLLED STUDY; DOG; DOSE RESPONSE; DRUG SAFETY; ELECTRORETINOGRAPHY; GENE MUTATION; GENE TRANSFER; GENETIC HETEROGENEITY; HISTOPATHOLOGY; LEBER CONGENITAL AMAUROSIS; MONKEY; NONHUMAN; OPTIC NERVE; PARVOVIRUS VECTOR; RETINA; RETINA DEGENERATION; RETINA FOVEA; RETINA INJURY; RPE65 GENE; TOXICITY TESTING; VITREOUS BODY; ADENO ASSOCIATED VIRUS; ANIMAL; BRAIN; GENE THERAPY; GENETICS; HUMAN; LEBER HEREDITARY OPTIC NEUROPATHY; MACACA; METABOLISM; MUTATION; PATHOLOGY; PHOTORECEPTOR; VIROLOGY;

ANIMALIA; CANIS FAMILIARIS; MACACA FASCICULARIS; PRIMATES;

ANIMALS; BLINDNESS; BRAIN; CARRIER PROTEINS; DEPENDOVIRUS; DOGS; EYE PROTEINS; GENE THERAPY; HUMANS; MACACA FASCICULARIS; MUTATION; OPTIC ATROPHY, HEREDITARY, LEBER; OPTIC NERVE; PHOTORECEPTORS; RETINA;

EID: 33750591238     PISSN: 10430342     EISSN: None     Source Type: Journal    
DOI: 10.1089/hum.2006.17.845     Document Type: Article

References (43)

1. ACLAND, G.M., AGUIRRE, G.D., RAY, J., ZHANG, Q., ALEMAN, T.S., CIDECIYAN, A.V., PEARCE-KELLING, S.E., ANAND, V., ZENG, Y., MAGUIRE, A.M., JACOBSON, S.G., HAUSWIRTH, W.W., and BENNETT, J. (2001). Gene therapy restores vision in a canine model of childhood blindness. Nat. Genet. 28, 92-95.
2. ACLAND, G.M., AGUIRRE, G.D., BENNETT, J., ALEMAN, T.S., CIDECIYAN, A.V., BENNICELLI, J., DEJNEKA, N.S., PEARCE-KELLING, S.E., MAGUIRE, A.M., PALCZEWSKI, K., HAUSWIRTH, W.W., and JACOBSON, S.G. (2005). Long-term restoration of rod and cone vision by single dose rAAV-mediated gene transfer to the retina in a canine model of childhood blindness. Mol. Ther. 12, 1072-1082.
3. AURICCHIO, A., and ROLLING, F. (2005). Adeno-associated viral vectors for retinal gene transfer and treatment of retinal diseases. Curr. Gene Ther. 5, 339-348.
4. BATTEN, M.L., IMANISHI, Y., TU, D.C., DOAN, T., ZHU, L., PANG, J., GLUSHAKOVA, L., MOISE, A.R., BAEHR, W., GELDER, R.N., HAUSWIRTH, W.W., RIEKE, F., and PALCZEWSKI, K. (2005). Pharmacological and rAAV gene therapy rescue of visual functions in a blind mouse model of Leber congenital amaurosis. PLoS Med. 2, e333.
5. BENNETT, J., MAGUIRE, A.M., CIDECIYAN, A.V., SCHNELL, M., GLOVER, E., ANAND, V., ALEMAN, T.S., CHIRMULE, N., GUPTA, A.R., HUANG, Y., GAO, G.P., NYBERG, W.C., TAZELAAR, J., HUGHES, J., WILSON, J.M., and JACOBSON, S.G. (1999). Stable transgene expression in rod photoreceptors after recombinant adeno-associated virus-mediated gene transfer to monkey retina. Proc. Natl. Acad. Sci. U.S.A. 96, 9920-9925.
6. COUTO, L.B. (2004). Preclinical gene therapy studies for hemophilia using adeno-associated virus (AAV) vectors. Semin. Thromb. Hemost. 30, 161-171.
7. CREMERS, F.P., VAN DEN HURK, J.A., and DEN HOLLANDER, A.I. (2002). Molecular genetics of Leber congenital amaurosis. Hum. Mol. Genet. 11, 1169-1176.
8. CURCIO, C.A., SLOAN, K.R., KALINA, R.E., and HENDRICKSON, A.E. (1990). Human photoreceptor topography. J. Comp. Neurol. 292, 497-523.
9. DEJNEKA, N.S., SURACE, E.M., ALEMAN, T.S., CIDECIYAN, A.V., LYUBARSKY, A., SAVCHENKO, A., REDMOND, T.M., TANG, W., WEI, Z., REX, T.S., GLOVER, E., MAGUIRE, A.M., PUGH, E.N., Jr., JACOBSON, S.G., and BENNETT, J. (2004). In utero gene therapy rescues vision in a murine model of congenital blindness. Mol. Ther. 9, 182-188.
10. DINCULESCU, A., GLUSHAKOVA, L., MIN, S.H., and HAUSWIRTH, W.W. (2005). Adeno-associated virus-vectored gene therapy for retinal disease. Hum. Gene Ther. 16, 649-663.
11. DONSANTE, A., VOGLER, C., MUZYCZKA, N., CRAWFORD, J.M., BARKER, J., FLOTTE, T., CAMPBELL-THOMPSON, M., DALY, T., and SANDS, M.S. (2001). Observed incidence of tumorigenesis in long-term rodent studies of rAAV vectors. Gene Ther. 8, 1343-1346.
12. FLOTTE, T.R. (2005). Adeno-associated virus-mediated gene transfer for lung diseases. Hum. Gene Ther. 16, 643-648.
13. HARE, W.A., WOLDEMUSSIE, E., WEINREB, R.N., TON, H., RUIZ, G., WIJONO, M., FELDMANN, B., ZANGWILL, L., and WHEELER, L. (2004). Efficacy and safety of memantine treatment for reduction of changes associated with experimental glaucoma in monkey. II. Structural measures. Invest. Ophthalmol. Vis. Sci. 45, 2640-2651.
14. HOGAN, M.J., ALVARADO, J.A., and WEDDELL, J.E. (1971). Histology of the Human Eye. (WB Saunders, Philadelphia, PA) pp. 393-522.
15. JACOBSON, S.G., YAGASAKI, K., FEUER, W.J., and ROMAN, A.J. (1989). Interocular asymmetry of visual function in heterozygotes of X-linked retinitis pigmentosa. Exp. Eye Res. 48, 679-691.
16. JACOBSON, S.G., MORALES, D.S., SUN, X.K., FEUER, W.J., CIDECIYAN, A.V., GASS, J.D., and MILAM, A.H. (1995). Pattern of retinal dysfunction in acute zonal occult outer retinopathy. Ophthalmology 102, 1187-1198.
17. JACOBSON, S.G., ALEMAN, T.S., CIDECIYAN, A.V., SUMAROKA, A., SCHWARTZ, S.B., WINDSOR, E.A., TRABOULSI, E.I., HEON, E., PITTLER, S.J., MILAM, A.H., MAGUIRE, A.M., PALCZEWSKI, K., STONE, E.M., and BENNETT, J. (2005). Identifying photoreceptors in blind eyes caused by RPE65 mutations: Prerequisite for human gene therapy success. Proc. Natl. Acad. Sci. U.S.A. 102, 6177-6182.
18. JACOBSON, S.G., ACLAND, G.M., AGUIRRE, G.D., ALEMAN, T.S., SCHWARTZ, S.B., CIDECIYAN, A.V., ZEISS, C.J., KOMAROMY, A.M., KAUSHAL, S., ROMAN, A.J., WINDSOR, E.A.M., SUMAROKA, A., PEARCE-KELLING, S.E., CONLON, T.J., CHIODO, V.A., BOYE, S.L., FLOTTE, T.R., MAGUIRE, A.M., BENNETT, J., and HAUSWIRTH, W.W. (2006). Safety of recombinant adeno-associated virus type 2-RPE65 vector delivered by ocular subretinal injection. Mol. Ther. 13, 1074-1084.
19. JIN, M., LI, S., MOGHRABI, W.N., SUN, H., and TRAVIS, G.H. (2005). Rpe65 is the retinoid isomerase in bovine retinal pigment epithelium. Cell 122, 449-459.
20. KENNAN, A., AHERNE, A., and HUMPHRIES, P. (2005). Light in retinitis pigmentosa. Trends Genet. 21, 103-110.
21. -/- knockout mouse eye results in limited rescue. Genet. Vaccines Ther. 2, 3.
22. LA VAIL, M.M., YASUMURA, D., MATTHES, M.T., DRESNER, K.A., FLANNERY, J.G., LEWIN, A.S., and HAUSWIRTH, W.W. (2000). Ribozyme rescue of photoreceptor cells in P23H transgenic rats: Long-term survival and late-stage therapy. Proc. Natl. Acad. Sci. U.S.A. 97, 11488-11493.
23. LE MEUR, G., WEBER, M., PEREON, Y., MENDES-MADEIRA, A., NIVARD, D., DESCHAMPS, J.Y., MOULLIER, P., and ROLLING, F. (2005). Postsurgical assessment and long-term safety of recombinant adeno-associated virus-mediated gene transfer into the retinas of dogs and primates. Arch. Ophthalmol. 123, 500-506.
24. LEUNG, I.Y., SANDSTROM, M.M., ZUCKER, C.L., NEURINGER, M., and MAX SNODDERLY, D. (2005). Nutritional manipulation of primate retinas. IV. Effects of n-3 fatty acids, lutein, and zeaxanthin on S-cones and rods in the foveal region. Exp. Eye Res, 81, 513-529.
25. MARMOR, M.F., HOLDER, G.E., SEELIGER, M.W., YAMAMOTO, S., and INTERNATIONAL SOCIETY FOR CLINICAL ELECTROPHYSIOLOGY OF VISION. Standard for clinical electroretinography (2004 update). Doc. Ophthalmol. 108, 107-114.
26. MOISEYEV, G., CHEN, Y., TAKAHASHI, Y., WU, B.X., and MA, J.X. (2005). RPE65 is the isomerohydrolase in the retinoid visual cycle. Proc. Natl. Acad. Sci. U.S.A. 102, 12413-12418.
27. NARFSTROM, K., KATZ, M.L., BRAGADOTTIR, R., SEELIGER, M., BOULANGER, A., REDMOND, T.M., CARO, L., LAI, C.M., and RAKOCZY, P.E. (2003). Functional and structural recovery of the retina after gene therapy in the RPE65 null mutation dog. Invest. Ophthalmol. Vis. Sci. 44, 1663-1672.
28. PANG, J.J., CHANG, B., KUMAR, A., NUSINOWITZ, S., NOORWEZ, S.M., LI, J., RANI, A., FOSTER, T.C., CHIODO, V.A., DOYLE, T., LI, H., MALHOTRA, R., TUSNER, I., McDOWELL, I.H., MIN, S.H., LI, Q., KAUSHAL, S., and HAUSWIRTH, W.W. (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.
29. PAWLYK, B.S., SMITH, A.I., BUCH, P.K., ADAMIAN, M., HONG, D.H., SANDBERG, M.A., ALI, R.R., and LI, T. (2005). Gene replacement therapy rescues photoreceptor degeneration in a murine model of Leber congenital amaurosis lacking RPGRIP. Invest. Ophthalmol. Vis. Sci. 46, 3039-3045.
30. POLYAK, S.L. (1941). The Retina. (University Chicago Press, Chicago, IL).
31. PREISING, M.N., and HEEGAARD, S. (2004). Recent advances in early-onset severe retinal degeneration: More than just basic research. Trends Mol. Med. 10, 51-54.
32. PROVIS, J.M., PENFOLD, P.L., CORNISH, E.E., SANDERCOE, T.M., and MADIGAN, M.C. (2005). Anatomy and development of the macula: Specialisation and the vulnerability to macular degeneration. Clin. Exp. Optom. 88, 269-281.
33. PROVOST, N., LE MEUR, G., WEBER, M., MENDES-MADEIRA, A., PODEVIN, G., CHEREL, Y., COLLE, M.A., DESCHAMPS, J.Y., MOULLIER, P., and ROLLING, F. (2005). Biodistribution of rAAV vectors following intraocular administration: Evidence for the presence and persistence of vector DNA in the optic nerve and in the brain. Mol. Ther. 11, 275-283.
34. RANDO, R.R. (2001). The biochemistry of the visual cycle. Chem. Rev. 101, 1881-1896.
35. REDMOND, T.M., YU, S., LEE, E., BOK, D., HAMASAKI, D., CHEN, N., GOLETZ, P., MA, J.X., CROUCH, R.K., and PFEIFER, K. (1998). Rpe65 is necessary for production of 11-cis-vitamin A in the retinal visual cycle. Nat. Genet. 20, 344-351.
36. REDMOND, T.M., POLIAKOV, E., YU, S., TSAI, J.Y., LU, Z., and GENTLEMAN, S. (2005). Mutation of key residues of RPE65 abolishes its enzymatic role as isomerohydrolase in the visual cycle. Proc. Natl. Acad. Sci. U.S.A. 102, 13658-13663.
37. ROBERTS, J.A., CLAYTON, J.D., and SEIBOLD, H.R. (1972). The natural incidence of pyelonephritis in the nonhuman primate. Invest. Urol. 9, 276-281.
38. ROLLING, F. (2004). Recombinant AAV-mediated gene transfer to the retina: Gene therapy perspectives. Gene Ther. 11, S26-S32.
39. SKELTON-STROUD, P.N., and GLAISTER, J.R. (1987). Naturally occurring renal disease in non-human primates. In: P.H. Bach and E.A. Lock, eds. Nephrotoxicity in the Experimental and Clinical Situation. (Martinus Nijhoff, New York) pp. 189-210.
40. SONG, S., SCOTT-JORGENSEN, M., WANG, J., POIRIER, A., CRAWFORD, J., CAMPBELL-THOMPSON, M., and FLOTTE, T.R. (2002). Intramuscular administration of recombinant adeno-associated virus 2 α-1 antitrypsin (rAAV-SERPINA1) vectors in a non-human primate model: Safety and immunologic aspects. Mol. Ther. 6, 329-335.
41. SURACE, E.M., and AURICCHIO, A. (2003). Adeno-associated viral vectors for retinal gene transfer. Prog. Retin. Eye Res. 22, 705-719.
42. SZLYK, J.P., FISHMAN, G.A., GROVER, S., REVELINS, B.I., and DERLACKI, D.J. (1998). Difficulty in performing everyday activities in patients with juvenile macular dystrophies: Comparison with patients with retinitis pigmentosa. Br. J. Ophthalmol. 82, 1372-1376.
43. THOMPSON, D.A., and GAL, A. (2003). Vitamin A metabolism in the retinal pigment epithelium: Genes, mutations, and diseases. Prog. Redn. Eye Res. 22, 683-703.