A novel method combining vitreous aspiration and intravitreal AAV2/8 injection results in retina-wide transduction in adult mice

Investigative Ophthalmology and Visual Science

Volumn 57, Issue 13, 2016, Pages 5326-5334

  Da Costa, Romain ^a   Röger, Carsten ^a   Segelken, Jasmin ^a   Barben, Maya ^b,c   Grimm, Christian ^b,c   Neidhardt, John ^a  

^a UNIVERSITY OF OLDENBURG   (Germany)

^b UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^c UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

AAV2 8; Intravitreal injection; Retinal degeneration; Retinal dystrophy; Viral vector

Indexed keywords

GREEN FLUORESCENT PROTEIN; PARVOVIRUS VECTOR;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTRORETINOGRAPHY; EYE FUNDUS; GENE REPLACEMENT THERAPY; GENE THERAPY; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; LASER MICROSCOPY; MOUSE; NONHUMAN; OPTICAL COHERENCE TOMOGRAPHY; PHOTOTRANSDUCTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA DEGENERATION; RETINA DYSTROPHY; TISSUE FIXATION; VITREORETINOPATHY; ADMINISTRATION AND DOSAGE; ANIMAL; C57BL MOUSE; CONFOCAL MICROSCOPY; DEPENDOPARVOVIRUS; DISEASE MODEL; GENE VECTOR; GENETIC TRANSDUCTION; GENETICS; INTRAVITREAL DRUG ADMINISTRATION; PATHOGENICITY; PATHOLOGY; PATHOPHYSIOLOGY; PIGMENT EPITHELIUM; PROCEDURES; RETINA; RETINAL DISEASES; SUCTION; TRANSGENE; VITREOUS BODY;

ANIMALS; DEPENDOVIRUS; DISEASE MODELS, ANIMAL; ELECTRORETINOGRAPHY; GENETIC THERAPY; GENETIC VECTORS; INTRAVITREAL INJECTIONS; MICE; MICE, INBRED C57BL; MICROSCOPY, CONFOCAL; PIGMENT EPITHELIUM OF EYE; RETINA; RETINAL DISEASES; SUCTION; TOMOGRAPHY, OPTICAL COHERENCE; TRANSDUCTION, GENETIC; TRANSGENES; VITREOUS BODY;

EID: 84994045458     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.16-19701     Document Type: Article

References (54)

1. Berger W, Kloeckener-Gruissem B, Neidhardt J. The molecular basis of human retinal and vitreoretinal diseases. Prog Retin Eye Res. 2010; 29: 335-375.
2. Boye SE, Boye SL, Lewin AS, Hauswirth WW. A comprehensive review of retinal gene therapy. Mol Ther. 2013; 21: 509-519.
3. Colella P, Cotugno G, Auricchio A. Ocular gene therapy: current progress and future prospects. Trends Mol Med. 2009; 15: 23-31.
4. Sahel JA, Roska B. Gene therapy for blindness. Annu Rev Neurosci. 2013; 36: 467-488.
5. McClements ME, MacLaren RE. Gene therapy for retinal disease. Transl Res. 2013; 161: 241-254.
6. Mingozzi F, High KA. Therapeutic in vivo gene transfer for genetic disease using AAV: progress and challenges. Nat Rev Genet. 2011; 12: 341-355.
7. Allocca M, Mussolino C, Garcia-Hoyos M, et al. Novel adenoassociated virus serotypes efficiently transduce murine photoreceptors. J Virol. 2007; 81: 11372-11380.
8. Lebherz C, Maguire A, Tang W, Bennett J, Wilson JM. Novel AAV serotypes for improved ocular gene transfer. J Gene Med. 2008; 10: 375-382.
9. Tan MH, Smith AJ, Pawlyk B, et al. Gene therapy for retinitis pigmentosa and Leber congenital amaurosis caused by defects in AIPL1: effective rescue of mouse models of partial and complete Aipl1 deficiency using AAV2/2 and AAV2/8 vectors. Hum Mol Genet. 2009; 18: 2099-2114.
10. Zou J, Luo L, Shen Z, et al. Whirlin replacement restores the formation of the USH2 protein complex in whirlin knockout photoreceptors. Invest Ophthalmol Vis Sci. 2011; 52: 2343-2351.
11. Seo S, Mullins RF, Dumitrescu AV, et al. Subretinal gene therapy of mice with Bardet-Biedl syndrome type 1. Invest Ophthalmol Vis Sci. 2013; 54: 6118-6132.
12. Birke MT, Lipo E, Adhi M, Birke K, Kumar-Singh R. AAVmediated expression of human PRELP inhibits complement activation, choroidal neovascularization and deposition of membrane attack complex in mice. Gene Ther. 2014; 21: 507-513.
13. Koilkonda R, Yu H, Talla V, et al. LHON gene therapy vector prevents visual loss and optic neuropathy induced by G11778A mutant mitochondrial DNA: biodistribution and toxicology profile. Invest Ophthalmol Vis Sci. 2014; 55: 7739-7753.
14. Choi VW, Bigelow CE, McGee TL, et al. AAV-mediated RLBP1 gene therapy improves the rate of dark adaptation in Rlbp1 knockout mice. Mol Ther Methods Clin Dev. 2015; 2: 15022.
15. Ou J, Vijayasarathy C, Ziccardi L, et al. Synaptic pathology and therapeutic repair in adult retinoschisis mouse by AAV-RS1 transfer. J Clin Invest. 2015; 125: 2891-2903.
16. Palfi A, Chadderton N, O’Reilly M, et al. Efficient gene delivery to photoreceptors using AAV2/rh10 and rescue of the Rho_/_ mouse. Mol Ther Methods Clin Dev. 2015; 2: 15016.
17. Xiong W, MacColl Garfinkel AE, Li Y, Benowitz LI, Cepko CL. NRF2 promotes neuronal survival in neurodegeneration and acute nerve damage. J Clin Invest. 2015; 125: 1433-1445.
18. Bainbridge JW, Smith AJ, Barker SS, et al. Effect of gene therapy on visual function in Leber’s congenital amaurosis. N Engl J Med. 2008; 358: 2231-2239.
19. Cideciyan AV, Aleman TS, Boye SL, 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. 2008; 105: 15112-15117.
20. Hauswirth WW, Aleman TS, Kaushal S, 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.
21. Maguire AM, Simonelli F, Pierce EA, et al. Safety and efficacy of gene transfer for Leber’s congenital amaurosis. N Engl J Med. 2008; 358: 2240-2248.
22. Cideciyan AV. Leber congenital amaurosis due to RPE65 mutations and its treatment with gene therapy. Prog Retin Eye Res. 2010; 29: 398-427.
23. MacLaren RE, Groppe M, Barnard AR, et al. Retinal gene therapy in patients with choroideremia: initial findings from a phase 1/2 clinical trial. Lancet. 2014; 383: 1129-1137.
24. Sakamoto T, Ueno H, Goto Y, Oshima Y, Ishibashi T, Inomata H. A vitrectomy improves the transfection efficiency of adenoviral vector-mediated gene transfer to Muller cells. Gene Ther. 1998; 5: 1088-1097.
25. Martin KR, Klein RL, Quigley HA. Gene delivery to the eye using adeno-associated viral vectors. Methods. 2002; 28: 267-275.
26. Acland GM, Aguirre GD, Bennett J, et al. 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. 2005; 12: 1072-1082.
27. Natkunarajah M, Trittibach P, McIntosh J, et al. Assessment of ocular transduction using single-stranded and self-complementary recombinant adeno-associated virus serotype 2/8. Gene Ther. 2008; 15: 463-467.
28. Pang JJ, Lauramore A, Deng WT, 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.
29. Hellstrom M, Ruitenberg MJ, Pollett MA, et al. Cellular tropism and transduction properties of seven adeno-associated viral vector serotypes in adult retina after intravitreal injection. Gene Ther. 2009; 16: 521-532.
30. Pechan P, Rubin H, Lukason M, et al. Novel anti-VEGF chimeric molecules delivered by AAV vectors for inhibition of retinal neovascularization. Gene Ther. 2009; 16: 10-16.
31. Prentice HM, Biswal MR, Dorey CK, Blanks JC. Hypoxiaregulated retinal glial cell-specific promoter for potential gene therapy in disease. Invest Ophthalmol Vis Sci. 2011; 52: 8562-8570.
32. Chadderton N, Palfi A, Millington-Ward S, et al. Intravitreal delivery of AAV-NDI1 provides functional benefit in a murine model of Leber hereditary optic neuropathy. Eur J Hum Genet. 2013; 21: 62-68.
33. Park TK, Wu Z, Kjellstrom S, et al. Intravitreal delivery of AAV8 retinoschisin results in cell type-specific gene expression and retinal rescue in the Rs1-KO mouse. Gene Ther. 2009; 16: 916-926.
34. Igarashi T, Miyake K, Asakawa N, Miyake N, Shimada T, Takahashi H. Direct comparison of administration routes for AAV8-mediated ocular gene therapy. Curr Eye Res. 2013; 38: 569-577.
35. Petrs-Silva H, Dinculescu A, Li Q, et al. High-efficiency transduction of the mouse retina by tyrosine-mutant AAV serotype vectors. Mol Ther. 2009; 17: 463-471.
36. Dalkara D, Kolstad KD, Guerin KI, et al. AAV mediated GDNF secretion from retinal glia slows down retinal degeneration in a rat model of retinitis pigmentosa. Mol Ther. 2011; 19: 1602-1608.
37. Ku CA, Chiodo VA, Boye SL, et al. Gene therapy using selfcomplementary Y733F capsid mutant AAV2/8 restores vision in a model of early onset Leber congenital amaurosis. Hum Mol Genet. 2011; 20: 4569-4581.
38. Dalkara D, Byrne LC, Klimczak RR, et al. In vivo-directed evolution of a new adeno-associated virus for therapeutic outer retinal gene delivery from the vitreous. Sci Transl Med. 2013; 5: 189ra176.
39. Kay CN, Ryals RC, Aslanidi GV, et al. Targeting photoreceptors via intravitreal delivery using novel, capsid-mutated AAV vectors. PLoS One. 2013; 8: e62097.
40. Grieger JC, Choi VW, Samulski RJ. Production and characterization of adeno-associated viral vectors. Nat Protoc. 2006; 1: 1412-1428.
41. Heynen SR, Tanimoto N, Joly S, Seeliger MW, Samardzija M, Grimm C. Retinal degeneration modulates intracellular localization of CDC42 in photoreceptors. Mol Vis. 2011; 17: 2934-2946.
42. Kranz K, Dorgau B, Pottek M, et al. Expression of Pannexin1 in the outer plexiform layer of the mouse retina and physiological impact of its knockout. J Comp Neurol. 2013; 521: 1119-1135.
43. Chiu K, Chang RC, So KF. Intravitreous injection for establishing ocular diseases model. J Vis Exp. 2007; 8: 313.
44. Fisher SK, Lewis GP, Linberg KA, Verardo MR. Cellular remodeling in mammalian retina: results from studies of experimental retinal detachment. Prog Retin Eye Res. 2005; 24: 395-431.
45. Sakai T, Tsuneoka H, Lewis GP, Fisher SK. Remodelling of retinal on- and off-bipolar cells following experimental retinal detachment. Clin Experiment Ophthalmol. 2014; 42: 480-485.
46. Dalkara D, Kolstad KD, Caporale N, et al. Inner limiting membrane barriers to AAV-mediated retinal transduction from the vitreous. Mol Ther. 2009; 17: 2096-2102.
47. Akache B, Grimm D, Pandey K, Yant SR, Xu H, Kay MA. The 37/67-kilodalton laminin receptor is a receptor for adenoassociated virus serotypes 8 2, 3, and 9. J Virol. 2006; 80: 9831-9836.
48. Mbazima V, Dias BD, Omar A, Jovanovic K, Weiss SFT. Interactions between PrPc and other ligands with the 37- kDa/67-kDa laminin receptor. Front Biosci (Landmark Ed). 2010; 15: 1150-1163.
49. Kotterman MA, Yin L, Strazzeri JM, Flannery JG, Merigan WH, Schaffer DV. Antibody neutralization poses a barrier to intravitreal adeno-associated viral vector gene delivery to non-human primates. Gene Ther. 2015; 22: 116-126.
50. Gupta V, Arevalo JF. Surgical management of diabetic retinopathy. Middle East Afr J Ophthalmol. 2013; 20: 283-292.
51. Bahadir M, Ertan A, Mertoglu O. Visual acuity comparison of vitrectomy with and without internal limiting membrane removal in the treatment of diabetic macular edema. Int Ophthalmol. 2005; 26: 3-8.
52. Da Mata AP, Burk SE, Foster RE, et al. Long-term follow-up of indocyanine green-assisted peeling of the retinal internal limiting membrane during vitrectomy surgery for idiopathic macular hole repair. Ophthalmology. 2004; 111: 2246-2253.
53. Ikuno Y, Sayanagi K, Ohji M, et al. Vitrectomy and internal limiting membrane peeling for myopic foveoschisis. Am J Ophthalmol. 2004; 137: 719-724.
54. Boyd RF, Boye SL, Conlon TJ, et al. Reduced retinal transduction and enhanced transgene-directed immunogenicity with intravitreal delivery of rAAV following posterior vitrectomy in dogs. Gene Ther. 2016; 23: 548-556.