Retinal gene therapy with a large MYO7A cDNA using adeno-associated virus

Gene Therapy

Volumn 20, Issue 8, 2013, Pages 824-833

  Lopes, V S ^a,b   Boye, S E ^a   Louie, C M ^a   Boye, S ^a   Dyka, F ^a   Chiodo, V ^a   Fofo, H ^b   Hauswirth, W W ^a   Williams, D S ^a  

^a JULES STEIN EYE INSTITUTE   (United States)

^b UNIVERSITY OF COIMBRA   (Portugal)

Author keywords

adeno associated virus; gene therapy; MYO7A; retina; RPE; Usher syndrome

Indexed keywords

COMPLEMENTARY DNA; MYOSIN VIIA; PARVOVIRUS VECTOR; PLASMID VECTOR; SCOTOPSIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL CULTURE; CELLULAR DISTRIBUTION; GENE INSERTION; HOMOLOGOUS RECOMBINATION; IMMUNOELECTRON MICROSCOPY; IMMUNOFLUORESCENCE; IMMUNOGOLD LABELING; MELANOSOME; MOUSE; NONHUMAN; PHENOTYPE; PHOTORECEPTOR CELL; PHOTORECEPTOR CONNECTING CILIUM; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA CELL; RETINAL GENE THERAPY; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY; WESTERN BLOTTING;

ANIMALS; DEPENDOVIRUS; DNA, COMPLEMENTARY; GENE EXPRESSION; GENE TRANSFER TECHNIQUES; GENETIC THERAPY; GREEN FLUORESCENT PROTEINS; HUMANS; MICE; MYOSINS; RETINA; RETINAL DEGENERATION; USHER SYNDROMES;

ADENO-ASSOCIATED VIRUS; MUS;

EID: 84881477796     PISSN: 09697128     EISSN: 14765462     Source Type: Journal    
DOI: 10.1038/gt.2013.3     Document Type: Article

References (53)

1. Bainbridge JW, Smith AJ, Barker SS, Robbie S, Henderson R, Balaggan K et al. Effect of gene therapy on visual function in Leber's congenital amaurosis. N Engl J Med 2008; 358: 2231-2239.
2. Maguire AM, Simonelli F, Pierce EA, Pugh Jr. EN, Mingozzi F, Bennicelli J et al. Safety and efficacy of gene transfer for Leber's congenital amaurosis. N Engl J Med 2008; 358: 2240-2248.
3. Hauswirth WW, Aleman TS, Kaushal S, Cideciyan AV, Schwartz SB, Wang L et al. 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 2008; 19: 979-990.
4. Cideciyan AV, Aleman TS, Boye SL, Schwartz SB, Kaushal S, Roman AJ et al. Human gene therapy for RPE65 isomerase deficiency activates the retinoid cycle of vision but with slow rod kinetics. Proc Natl Acad Sci USA 2008; 105: 15112-15117.
5. Weil D, Blanchard S, Kaplan J, Guilford P, Gibson F, Walsh J et al. Defective myosin VIIA gene responsible for Usher syndrome type 1B. Nature 1995; 374: 60-61.
6. Liu X, Ondek B, Williams DS. Mutant myosin VIIa causes defective melanosome distribution in the RPE of shaker-1 mice. Nat Genet 1998; 19: 117-118.
7. Liu X, Udovichenko IP, Brown SDM, Steel KP, Williams DS. Myosin VIIa participates in opsin transport through the photoreceptor cilium. J Neurosci 1999; 19: 6267-6274.
8. Gibbs D, Kitamoto J, Williams DS. Abnormal phagocytosis by retinal pigmented epithelium that lacks myosin VIIa, the Usher syndrome 1B protein. Proc Natl Acad Sci USA 2003; 100: 6481-6486.
9. Gibbs D, Azarian SM, Lillo C, Kitamoto J, Klomp AE, Steel KP et al. Role of myosin VIIa and Rab27a in the motility and localization of RPE melanosomes. J Cell Sci 2004; 117: 6473-6483.
10. Lopes VS, Gibbs D, Libby RT, Aleman TS, Welch DL, Lillo C et al. The Usher 1B protein, MYO7A, is required for normal localization and function of the visual retinoid cycle enzyme, RPE65. Hum Mol Genet 2011; 20: 2560-2570.
11. Williams DS, Lopes VS. The many different cellular functions of MYO7A in the retina. Biochem Soc Trans 2011; 39: 1207-1210.
12. Jacobson SG, Cideciyan AV, Gibbs D, Sumaroka A, Roman AJ, Aleman TS et al. Retinal disease course in Usher syndrome 1B due to MYO7A mutations. Invest Ophthalmol Vis Sci 2011; 52: 7924-7936.
13. Chen ZY, Hasson T, Kelley PM, Schwender BJ, Schwartz MF, Ramakrishnan M et al. Molecular cloning and domain structure of human myosin-VIIa, the gene product defective in Usher syndrome 1B. Genomics 1996; 36: 440-448.
14. Weil D, Levy G, Sahly I, Levi-Acobas F, Blanchard S, El-Amraoui A et al. Human myosin VIIA responsible for the Usher 1B syndrome: a predicted membraneassociated motor protein expressed in developing sensory epithelia. Proc Natl Acad Sci USA 1996; 93: 3232-3237.
15. Bowles DE, McPhee SW, Li C, Gray SJ, Samulski JJ, Camp AS et al. Phase 1 gene therapy for Duchenne muscular dystrophy using a translational optimized AAV vector. Mol Ther 2012; 20: 443-455.
16. Grieger JC, Samulski RJ. Packaging capacity of adeno-associated virus serotypes: impact of larger genomes on infectivity and postentry steps. J Virol 2005; 79: 9933-9944.
17. Hashimoto T, Gibbs D, Lillo C, Azarian SM, Legacki E, Zhang XM et al. Lentiviral gene replacement therapy of retinas in a mouse model for Usher syndrome type 1B. Gene Ther 2007; 14: 584-594.
18. Yang GS, Schmidt M, Yan Z, Lindbloom JD, Harding TC, Donahue BA et al. Virus-mediated transduction of murine retina with adeno-associated virus: effects of viral capsid and genome size. J Virol 2002; 76: 7651-7660.
19. Acland GM, Aguirre GD, Bennett J, Aleman TS, Cideciyan AV, Bennicelli J et al. Longterm 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 2005; 12: 1072-1082.
20. Allocca M, Doria M, Petrillo M, Colella P, Garcia-Hoyos M, Gibbs D et al. Serotypedependent packaging of large genes in adeno-associated viral vectors results in effective gene delivery in mice. J Clin Invest 2008; 118: 1955-1964.
21. Dong B, Nakai H, Xiao W. Characterization of genome integrity for oversized recombinant AAV vector. Mol Ther 2010; 18: 87-92.
22. Lai Y, Yue Y, Duan D. Evidence for the failure of adeno-associated virus serotype 5 to package a viral genome X 8.2 kb. Mol Ther 2010; 18: 75-79.
23. Wu Z, Yang H, Colosi P. Effect of genome size on AAV vector packaging. Mol Ther 2010; 18: 80-86.
24. Odom GL, Gregorevic P, Allen JM, Chamberlain JS. Gene therapy of mdx mice with large truncated dystrophins generated by recombination using rAAV6. Mol Ther 2011; 19: 36-45.
25. Zhang Y, Duan D. Novel mini-dystrophin gene dual adeno-associated virus vectors restore neuronal nitric oxide synthase expression at the sarcolemma. Hum Gene Ther 2012; 23: 98-103.
26. Haire SE, Pang J, Boye SL, Sokal I, Craft CM, Palczewski K et al. Light-driven cone arrestin translocation in cones of postnatal guanylate cyclase-1 knockout mouse retina treated with AAV-GC1. Invest Ophthalmol Vis Sci 2006; 47: 3745-3753.
27. Pang JJ, Lauramore A, Deng WT, Li Q, Doyle TJ, Chiodo V et al. Comparative analysis of in vivo and in vitro AAV vector transduction in the neonatal mouse retina: effects of serotype and site of administration. Vision Res 2008; 48: 377-385.
28. Hasson T, Heintzelman MB, Santos-Sacchi J, Corey DP, Mooseker MS. Expression in cochlea and retina of myosin VIIa, the gene product defective in Usher syndrome type 1B. Proc Natl Acad Sci USA 1995; 92: 9815-9819.
29. Liu X, Vansant G, Udovichenko IP, Wolfrum U, Williams DS. Myosin VIIa, the product of the Usher 1B syndrome gene, is concentrated in the connecting cilia of photoreceptor cells. Cell Motil Cytoskeleton 1997; 37: 240-252.
30. Williams DS. Usher syndrome: animal models, retinal function of Usher proteins, and prospects for gene therapy. Vision Res 2008; 48: 433-441.
31. Klomp AE, Teofilo K, Legacki E, Williams DS. Analysis of the linkage of MYRIP and MYO7A to melanosomes by RAB27A in retinal pigment epithelial cells. Cell Motil Cytoskeleton 2007; 64: 474-487.
32. Lopes VS, Ramalho JS, Owen DM, Karl MO, Strauss O, Futter CE et al. The ternary Rab27a-Myrip-Myosin VIIa complex regulates melanosome motility in the retinal pigment epithelium. Traffic 2007; 8: 486-499.
33. Bostick B, Shin JH, Yue Y, Duan D. AAV-microdystrophin therapy improves cardiac performance in aged female mdx mice. Mol Ther 2011; 19: 1826-1832.
34. Schwander M, Lopes V, Sczaniecka A, Gibbs D, Lillo C, Delano D et al. A novel allele of myosin VIIa reveals a critical function for the C-terminal FERM domain for melanosome transport in retinal pigment epithelial cells. J Neurosci 2009; 29: 15810-15818.
35. Yang Y, Baboolal TG, Siththanandan V, Chen M, Walker ML, Knight PJ et al. A FERM domain autoregulates Drosophila myosin 7a activity. Proc Natl Acad Sci USA 2009; 106: 4189-4194.
36. Wu L, Pan L, Wei Z, Zhang M. Structure of MyTH4-FERM domains in myosin VIIa tail bound to cargo. Science 2011; 331: 757-760.
37. Kapranov P, Chen L, Dederich D, Dong B, He J, Steinmann KE et al. Native molecular state of adeno-associated viral vectors revealed by single-molecule sequencing. Hum Gene Ther 2012; 23: 46-55.
38. Halbert CL, Allen JM, Miller AD. Efficient mouse airway transduction following recombination between AAV vectors carrying parts of a larger gene. Nat Biotechnol 2002; 20: 697-701.
39. Ghosh A, Yue Y, Duan D. Viral serotype and the transgene sequence influence overlapping adeno-associated viral (AAV) vector-mediated gene transfer in skeletal muscle. J Gene Med 2006; 8: 298-305.
40. Duan D, Yue Y, Engelhardt JF. Expanding AAV packaging capacity with trans-splicing or overlapping vectors: a quantitative comparison. Mol Ther 2001; 4: 383-391.
41. Ghosh A, Yue Y, Lai Y, Duan D. A hybrid vector system expands adeno-associated viral vector packaging capacity in a transgene-independent manner. Mol Ther 2008; 16: 124-130.
42. Auricchio A, Kobinger G, Anand V, Hildinger M, O'Connor E, Maguire AM et al. Exchange of surface proteins impacts on viral vector cellular specificity and transduction characteristics: the retina as a model. Hum Mol Genet 2001; 10: 3075-3081.
43. Allocca M, Manfredi A, Iodice C, Di Vicino U, Auricchio A. AAV-mediated gene replacement, either alone or in combination with physical and pharmacological agents, results in partial and transient protection from photoreceptor degeneration associated with betaPDE deficiency. Invest Ophthalmol Vis Sci 2011; 52: 5713-5719.
44. Zhong L, Li B, Mah CS, Govindasamy L, Agbandje-McKenna M, Cooper M et al. Next generation of adeno-associated virus 2 vectors: point mutations in tyrosines lead to high-efficiency transduction at lower doses. Proc Nat Acad Sci USA 2008; 105: 7827-7832.
45. Boye SL, Conlon T, Erger K, Ryals R, Neeley A, Cossette T et al. Long-term preservation of cone photoreceptors and restoration of cone function by gene therapy in the guanylate cyclase-1 knockout (GC1KO) mouse. Invest Ophthalmol Vis Sci 2011; 52: 7098-7108.
46. Pang JJ, Dai X, Boye SE, Barone I, Boye SL, Mao S et al. Long-term retinal function and structure rescue using capsid mutant AAV8 vector in the rd10 mouse, a model of recessive retinitis pigmentosa. Mol Ther 2011; 19: 234-242.
47. Hasson T, Walsh J, Cable J, Mooseker MS, Brown SDM, Steel KP. Effects of shaker-1 mutations on myosin-VIIa protein and mRNA expression. Cell Motil Cytoskeleton 1997; 37: 127-138.
48. Gibbs D, Diemer T, Khanobdee K, Hu J, Bok D, Williams DS. Function of MYO7A in the human RPE and the validity of shaker1 mice as a model for Usher syndrome 1B. Invest Ophthalmol Vis Sci 2010; 51: 1130-1135.
49. Gibson F, Walsh J, Mburu P, Varela A, Brown KA, Antonio M et al. A type VII myosin encoded by mouse deafness gene shaker-1. Nature 1995; 374: 62-64.
50. Zolotukhin S, Potter M, Zolotukhin I, Sakai Y, Loiler S, Fraites Jr. TJ et al. Production and purification of serotype 1, 2, and 5 recombinant adeno-associated viral vectors. Methods 2002; 28: 158-167.
51. Jacobson SG, Acland GM, Aguirre GD, Aleman TS, Schwartz SB, Cideciyan AV et al. Safety of recombinant adeno-associated virus type 2-RPE65 vector delivered by ocular subretinal injection. Mol Ther 2006; 13: 1074-1084.
52. Gibbs D, Williams DS. Isolation and culture of primary mouse retinal pigmented epithlelial cells. Adv Exp Med Biol 2003; 533: 347-352.
53. Soni LE, Warren CM, Bucci C, Orten DJ, Hasson T. The unconventional myosin-VIIa associates with lysosomes. Cell Motil Cytoskeleton 2005; 62: 13-26.