Proof of concept for AAV2/5-mediated gene therapy in iPSC-derived retinal pigment epithelium of a choroideremia patient

Molecular Therapy Methods and Clinical Development

Volumn 1, Issue , 2014, Pages 14011-

  Cereso, Nicolas ^a,b   Pequignot, Marie O ^a,b   Robert, Lorenne ^a,b   Becker, Fabienne ^a   De Luca, Valerie ^a,b   Nabholz, Nicolas ^a,b,d   Rigau, Valerie ^d   De Vos, John ^b,c,d   Hamel, Christian P ^a,b,d   Kalatzis, Vasiliki ^a,b  

^a Montpellier University Medical Center   (France)

^b UNIV MONTPELLIER   (France)

^c INSERM   (France)

^d MONTPELLIER UNIVERSITY HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84932084122     PISSN: None     EISSN: 23290501     Source Type: Journal    
DOI: 10.1038/mtm.2014.11     Document Type: Article

References (50)

1. Berger, W, Kloeckener-Gruissem, B and Neidhardt, J (2010). The molecular basis of human retinal and vitreoretinal diseases. Prog Retin Eye Res 29: 335-375.
2. Lipinski, DM, Thake, M and MacLaren, RE (2013). Clinical applications of retinal gene therapy. Prog Retin Eye Res 32: 22-47.
3. Colella, P, Cotugno, G and Auricchio, A (2009). Ocular gene therapy: current progress and future prospects. Trends Mol Med 15: 23-31.
4. 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.
5. Maguire, AM, Simonelli, F, Pierce, EA, Pugh, EN Jr, Mingozzi, F, Bennicelli, J et al. (2008). Safety and efficacy of gene transfer for Leber's congenital amaurosis. N Engl J Med 358: 2240-2248.
6. Hauswirth, WW, Aleman, TS, Kaushal, S, Cideciyan, AV, Schwartz, SB, Wang, L 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.
7. Maguire, AM, High, KA, Auricchio, A, Wright, JF, Pierce, EA, Testa, F et al. (2009). Age-dependent effects of RPE65 gene therapy for Leber's congenital amaurosis: a phase 1 dose-escalation trial. Lancet 374: 1597-1605.
8. 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 efficac y in 15 children and adults followed up to 3 years. A rch Ophthalmol 130: 9-24.
9. 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.
10. Marlhens, F, Bareil, C, Griffoin, JM, Zrenner, E, Amalric, P, Eliaou, C et al. (1997). Mutations in RPE65 cause Leber's congenital amaurosis. Nat Genet 17: 139-141.
11. Cottet, S, Michaut, L, Boisset, G, Schlecht, U, Gehring, W and Schorderet, DF (2006). Biological characterization of gene response in Rpe65-/-mouse model of Leber's congenital amaurosis during progression of the disease. FASEB J 20: 2036-2049.
12. Pang, JJ, Chang, B, Hawes, NL, Hurd, RE, Davisson, MT, Li, J et al. (2005). Retinal degeneration 12 (rd12): a new, spontaneously arising mouse model for human Leber congenital amaurosis (LCA). Mol Vis 11: 152-162.
13. Aguirre, GD, Baldwin, V, Pearce-Kelling, S, Narfström, K, Ray, K and Acland, GM (1998). Congenital stationary night blindness in the dog: common mutation in the RPE65 gene indicates founder effect. Mol Vis 4: 23.
14. Williams, DS (2008). Usher syndrome: animal models, retinal function of Usher proteins, and prospects for gene therapy. Vision Res 48: 433-441.
15. Sahly, I, Dufour, E, Schietroma, C, Michel, V, Bahloul, A, Perfettini, I et al. (2012). Localization of Usher 1 proteins to the photoreceptor calyceal processes, which are absent from mice. J Cell Biol 199: 381-399.
16. Tsai, KL, Clark, LA and Murphy, KE (2007). Understanding hereditary diseases using the dog and human as companion model systems. Mamm Genome 18: 444-451.
17. Bocquet, B, Lacroux, A, Surget, MO, Baudoin, C, Marquette, V, Manes, G et al. (2013). Relative frequencies of inherited retinal dystrophies and optic neuropathies in Southern France: assessment of 21-year data management. Ophthalmic Epidemiol 20: 13-25.
18. Seabra, MC, Brown, MS, Slaughter, CA, Südhof, TC and Goldstein, JL (1992). Purification of component A of Rab geranylgeranyl transferase: possible identity with the choroideremia gene product. Cell 70: 1049-1057.
19. van den Hurk, JA, Hendriks, W, van de Pol, DJ, Oerlemans, F, Jaissle, G, Rüther, K et al. (1997). Mouse choroideremia gene mutation causes photoreceptor cell degeneration and is not transmitted through the female germline. Hum Mol Genet 6: 851-858.
20. Shi, W, van den Hurk, JA, Alamo-Bethencourt, V, Mayer, W, Winkens, HJ, Ropers, HH et al. (2004). Choroideremia gene product affects trophoblast development and vascularization in mouse extra-embryonic tissues. Dev Biol 272: 53-65.
21. Starr, CJ, Kappler, JA, Chan, DK, Kollmar, R and Hudspeth, AJ (2004). Mutation of the zebrafish choroideremia gene encoding Rab escort protein 1 devastates hair cells. Proc Natl Acad Sci USA 101: 2572-2577.
22. Robert, L, Sénéchal, A, Bocquet, B, Herbin, L, Chaudieu, G, Kalatzis, V et al. (2011). Screening for a canine model of choroideremia exclusively identifies nonpathogenic CHM variants. Ophthalmic Res 45: 155-163.
23. Tolmachova, T, Anders, R, Abrink, M, Bugeon, L, Dallman, MJ, Futter, CE et al. (2006). Independent degeneration of photoreceptors and retinal pigment epithelium in conditional knockout mouse models of choroideremia. J Clin Invest 116: 386-394.
24. Tolmachova, T, Wavre-Shapton, ST, Barnard, AR, MacLaren, RE, Futter, CE and Seabra, MC (2010). Retinal pigment epithelium defects accelerate photoreceptor degeneration in cell type-specific knockout mouse models of choroideremia. Invest Ophthalmol Vis Sci 51: 4913-4920.
25. Tolmachova, T, Tolmachov, OE, Wavre-Shapton, ST, Tracey-White, D, Futter, CE and Seabra, MC (2012). CHM/REP1 cDNA delivery by lentiviral vectors provides functional expression of the transgene in the retinal pigment epithelium of choroideremia mice. J Gene Med 14: 158-168.
26. Nishikawa, S, Goldstein, RA and Nierras, CR (2008). The promise of human induced pluripotent stem cells for research and therapy. Nat Rev Mol Cell Biol 9: 725-729.
27. Ramirez, JM, Bai, Q, Péquignot, M, Becker, F, Kassambara, A, Bouin, A et al. (2013). Side scatter intensity is highly heterogeneous in undifferentiated pluripotent stem cells and predicts clonogenic self-renewal. Stem Cells Dev 22: 1851-1860.
28. Seabra, MC, Ho, YK and Anant, JS (1995). Deficient geranylgeranylation of Ram/Rab27 in choroideremia. J Biol Chem 270: 24420-24427.
29. Yu, J and Thomson, JA (2008). Pluripotent stem cell lines. Genes Dev 22: 1987-1997.
30. Takahashi, K, Tanabe, K, Ohnuki, M, Narita, M, Ichisaka, T, Tomoda, K et al. (2007). Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131: 861-872.
31. Yu, J, Vodyanik, MA, Smuga-Otto, K, Antosiewicz-Bourget, J, Frane, JL, Tian, S et al. (2007). Induced pluripotent stem cell lines derived from human somatic cells. Science 318: 1917-1920.
32. Grimm, S (2004). The art and design of genetic screens: mammalian culture cells. Nat Rev Genet 5: 179-189.
33. Park, IH, Zhao, R, West, JA, Yabuuchi, A, Huo, H, Ince, TA et al. (2008). Reprogramming of human somatic cells to pluripotency with defined factors. Nature 451: 141-146.
34. Singh, R, Shen, W, Kuai, D, Martin, JM, Guo, X, Smith, MA et al. (2013). iPS cell modeling of Best disease: insights into the pathophysiology of an inherited macular degeneration. Hum Mol Genet 22: 593-607.
35. Egawa, N, Kitaoka, S, Tsukita, K, Naitoh, M, Takahashi, K, Yamamoto, T et al. (2012). Drug screening for ALS using patient-specific induced pluripotent stem cells. Sci Transl Med 4: 145ra104.
36. Tucker, BA, Park, IH, Qi, SD, Klassen, HJ, Jiang, C, Yao, J et al. (2011). Transplantation of adult mouse iPS cell-derived photoreceptor precursors restores retinal structure and function in degenerative mice. PLoS One 6: e18992.
37. Vandenberghe, LH and Auricchio, A (2012). Novel adeno-associated viral vectors for retinal gene therapy. Gene Ther 19: 162-168.
38. Weber, M, Rabinowitz, J, Provost, N, Conrath, H, Folliot, S, Briot, D et al. (2003). Recombinant adeno-associated virus serotype 4 mediates unique and exclusive long-term transduction of retinal pigmented epithelium in rat, dog, and nonhuman primate after subretinal delivery. Mol Ther 7: 774-781.
39. Allocca, M, Mussolino, C, Garcia-Hoyos, M, Sanges, D, Iodice, C, Petrillo, M et al. (2007). Novel adeno-associated virus serotypes efficiently transduce murine photoreceptors. J Virol 81: 11372-11380.
40. Mussolino, C, della Corte, M, Rossi, S, Viola, F, Di Vicino, U, Marrocco, E et al. (2011). AAV-mediated photoreceptor transduction of the pig cone-enriched retina. Gene Ther 18: 637-645.
41. Agbandje-McKenna, M and Kleinschmidt, J (2011). AAV capsid structure and cell interactions. Methods Mol Biol 807: 47-92.
42. Ellis, BL, Hirsch, ML, Barker, JC, Connelly, J P, Steininger, RJ 3rd and Porteus, MH (2013). A survey of ex vivo/in vitro transduction efficiency of mammalian primary cells and cell lines with Nine natural adeno-associated virus (AAV1-9) and one engineered adeno-associated virus serotype. Virol J 10: 74.
43. Sparrow, JR, Hicks, D and Hamel, CP (2010). The retinal pigment epithelium in health and disease. Curr Mol Med 10: 802-823.
44. Vandenberghe, LH, Bell, P, Maguire, AM, Cearley, CN, Xiao, R, Calcedo, R et al. (2011). Dosage thresholds for AAV2 and AAV8 photoreceptor gene therapy in monkey. Sci Transl Med 3: 88ra54.
45. Krock, BL, Bilotta, J and Perkins, BD (2007). Noncell-autonomous photoreceptor degeneration in a zebrafish model of choroideremia. Proc Natl Acad Sci USA 104: 4600-4605.
46. Tolmachova, T, Tolmachov, OE, Barnard, AR, de Silva, SR, Lipinski, DM, Walker, NJ et al. (2013). Functional expression of Rab escort protein 1 following AAV2-mediated gene delivery in the retina of choroideremia mice and human cells ex vivo. J Mol Med (Berl) 91: 825-837.
47. Vasireddy, V, Mills, JA, Gaddameedi, R, Basner-Tschakarjan, E, Kohnke, M, Black, AD et al. (2013). AAV-mediated gene therapy for choroideremia: preclinical studies in personalized models. PLoS One 8: e61396.
48. Liao, JL, Yu, J, Huang, K, Hu, J, Diemer, T, Ma, Z et al. (2010). Molecular signature of primary retinal pigment epithelium and stem-cell-derived RPE cells. Hum Mol Genet 19: 4229-4238.
49. Wu, YW, Alexandrov, K and Brunsveld, L (2007). Synthesis of a fluorescent analogue of geranylgeranyl pyrophosphate and its use in a high-throughput fluorometric assay for Rab geranylgeranyltransferase. Nat Protoc 2: 2704-2711.
50. Nguyen UTT, Wu Y, Goodall A and Alexandrov K (2010). Analysis of protein prenylation in vitro and in vivo using functionalized phosphoisoprenoids. Curr Protoc Prot Sci 62: 14.13.11-14.13.15.