Quantifying transduction efficiencies of unmodified and tyrosine capsid mutant AAV vectors in vitro using two ocular cell lines

Molecular Vision

Volumn 17, Issue , 2011, Pages 1090-1102

  Ryals, Renee C ^a   Boye, Sanford L ^a   Dinculescu, Astra ^a   Hauswirth, William W ^a   Boye, Shannon E ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

ADENO ASSOCIATED VIRUS 1 VECTOR; ADENO ASSOCIATED VIRUS 2 VECTOR; ADENO ASSOCIATED VIRUS 5 VECTOR; ADENO ASSOCIATED VIRUS 8 VECTOR; ENHANCED GREEN FLUORESCENT PROTEIN; GREEN FLUORESCENT PROTEIN; PARVOVIRUS VECTOR; TYROSINE; UNCLASSIFIED DRUG; VIRUS VECTOR;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL SPECIFICITY; CONTROLLED STUDY; FLUORESCENCE ACTIVATED CELL SORTING; FLUORESCENCE ANALYSIS; GENETIC TRANSDUCTION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MICROSCOPY; MOUSE; NONHUMAN; NONVIRAL GENE THERAPY; PHOTORECEPTOR CELL; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROMOTER REGION; RETINA CONE; RETINA ROD; VIRAL GENE DELIVERY SYSTEM; VIRUS CAPSID; VIRUS CELL INTERACTION; VIRUS MUTANT; VIRUS MUTATION;

ANIMALS; CAPSID; CELL LINE; DEPENDOVIRUS; EPITHELIAL CELLS; FLOW CYTOMETRY; GENE THERAPY; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; MICE; PHENYLALANINE; PHOTORECEPTOR CELLS; RECOMBINANT FUSION PROTEINS; RETINA; TRANSFORMATION, GENETIC; TRANSGENES; TYROSINE; VISION, OCULAR;

EID: 79955602297     PISSN: None     EISSN: 10900535     Source Type: Journal    
DOI: None     Document Type: Article

References (50)

1. Bainbridge JW, Smith AJ, Barker SS, Robbie S, Henderson R, Balaggan K, Viswanathan A, Holder GE, Stockman A, Tyler N, Petersen-Jones S, Bhattacharya SS, Thrasher AJ, Fitzke FW, Carter BJ, Rubin GS, Moore AT, Ali RR. Effect of gene therapy on visual function in Leber's congenital amaurosis. N Engl J Med 2008; 358:2231-2239. [PMID: 18441371]
2. Cideciyan AV, Aleman TS, Boye SL, Schwartz SB, Kaushal S, Roman AJ, Pang JJ, Sumaroka A, Windsor EA, Wilson JM, Flotte TR, Fishman GA, Heon E, Stone EM, Byrne BJ, Jacobson SG, Hauswirth WW. 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. [PMID: 18809924]
3. Hauswirth WW, Aleman TS, Kaushal S, Cideciyan AV, Schwartz SB, Wang L, Conlon TJ, Boye SL, Flotte TR, Byrne BJ, Jacobson SG. 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. [PMID: 18774912]
4. Maguire AM, Simonelli F, Pierce EA, Pugh EN Jr, Mingozzi F, Bennicelli J, Banfi S, Marshall KA, Testa F, Surace EM, Rossi S, Lyubarsky A, Arruda VR, Konkle B, Stone E, Sun J, Jacobs J, Dell'Osso L, Hertle R, Ma JX, Redmond TM, Zhu X, Hauck B, Zelenaia O, Shindler KS, Maguire MG, Wright JF, Volpe NJ, McDonnell JW, Auricchio A, High KA, Bennett J. Safety and efficacy of gene transfer for Leber's congenital amaurosis. N Engl J Med 2008; 358:2240-2248. [PMID:18441370]
5. Komáromy AM, Alexander JJ, Rowlan JS, Garcia MM, Chiodo VA, Kaya A, Tanaka JC, Acland GM, Hauswirth WW, Aguirre GD. Gene therapy rescues cone function in congenital achromatopsia. Hum Mol Genet 2010; 19:2581-2593. [PMID: 20378608]
6. Alexander JJ, Umino Y, Everhart D, Chang B, Min SH, Li Q, Timmers AM, Hawes NL, Pang JJ, Barlow RB, Hauswirth WW. Restoration of cone vision in a mouse model of achromatopsia. Nat Med 2007; 13:685-687. [PMID: 17515894]
7. Mancuso K, Hauswirth WW, Li Q, Connor TB, Kuchenbecker JA, Mauck MC, Neitz J, Neitz M. Gene therapy for red-green colour blindness in adult primates. Nature 2009; 461:784-787. PMID: 19759534]
8. Boye SE, Boye SL, Pang J, Ryals R, Everhart D, Umino Y, Neeley AW, Besharse J, Barlow R, Hauswirth WW. Functional and behavioral restoration of vision by gene therapy in the guanylate cyclase-1 (GC1) knockout mouse. PLoS ONE 2010; 5:e11306. [PMID: 20593011]
9. Dunn KC, Aotaki-Keen AE, Putkey FR, Hjelmeland LM. ARPE-19, A Human Retinal Pigment Epithelial Cell Line with Differentiated Properties. Exp Eye Res 1996; 62:155-169. [PMID: 8698076]
10. Mandal MN, Patlolla JM, Zheng L, Agbaga MP, Tran JT, Wicker L, Kasus-Jacobi A, Elliott MH, Rao CV, Anderson RE. Curcumin protects retinal cells from light-and oxidant stress-induced cell death. Free Radic Biol Med 2009; 46:672-679. [PMID: 19121385]
11. Malek G, Hu P, Wielgus A, Dwyer M, Cousins S. PPAR Nuclear Receptors and Altered RPE Lipid Metabolism in Age-Related Macular Degeneration. Adv Exp Med Biol 2010; 664:429-436. [PMID: 20238044]
12. Steindl-Kuscher K, Krugluger W, Boulton ME, Haas P, Schrattbauer K, Feichtinger H, Adlassnig W, Binder S. Activation of the beta-catenin signaling pathway and its impact on RPE cell cycle. Invest Ophthalmol Vis Sci 2009; 50:4471-4476. [PMID: 19369241]
13. Mukherjee PK, Marcheselli VL, de Rivero Vaccari JC, Gordon WC, Jackson FE, Bazan NG. Photoreceptor outer segment phagocytosis attenuates oxidative stress-induced apoptosis with concomitant neuroprotectin D1 synthesis. Proc Natl Acad Sci USA 2007; 104:13158-13163. [PMID: 17670935]
14. Mannermaa E, Reinisalo M, Ranta VP, Vellonen KS, Kokki H, Saarikko A, Kaarniranta K, Urtti A. Filter-cultured ARPE-19 cells as outer blood-retinal barrier model. Eur J Pharm Sci 2010; 40:289-296.[PMID: 20385230]
15. Ablonczy Z, Prakasam A, Fant J, Fauq A, Crosson C, Sambamurti K. Pigment epithelium-derived factor maintains retinal pigment epithelium function by inhibiting vascular endothelial growth factor-R2 signaling through gammasecretase. J Biol Chem 2009; 284:30177-30186. [PMID: 19723623]
16. Al-Ubaidi MR, Matsumoto H, Kurono S, Singh A. Proteomics Profiling of the Cone Photoreceptor Cell Line, 661W. Adv Exp Med Biol 2008; 613:301-311. [PMID: 18188958]
17. Tan E, Din XQ, Saadi A, Agarwal N, Naash MI, Al-Ubaidi MR. Expressing of cone-photoreceptor-specific antigens in a cell line derived from retinal tumors in transgenic mice. Invest Ophthalmol Vis Sci 2004; 45:764-768. [PMID: 14985288]
18. Groeger G, Mackey AM, Pettigrew CA, Bhatt L, Cotter TG. Stress-induced activation of Nox contributes to cell survival signalling via production of hydrogen peroxide. J Neurochem 2009; 109:1544-1554. [PMID: 19344371]
19. Petrs-Silva H, Dinculescu A, Li Q, Min SH, Chiodo V, Pang JJ, Zhong L, Zolotukhin S, Srivastava A, Lewin AS, Hauswirth WW. High-efficiency transduction of the mouse retina by tyrosine-mutant AAV serotype vectors. Mol Ther 2009; 17:463-471. [PMID: 19066593]
20. Pang JJ, Dai X, Boye SE, Barone I, Boye SL, Mao S, Everhart D, Dinculescu A, Liu L, Umino Y, Lei B, Chang B, Barlow R, Strettoi E, Hauswirth WW. 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. [PMID: 21139570]
21. Haire SE, Pang J, Boye SL, Sokal I, Craft CM, Palczewski K, Hauswirth WW, Semple-Rowland SL. Light-driven cone arrestin translocation in cones of postnatal guanylatecyclase-1 knockout mouse retina treated with AAV-GC1. Invest Ophthalmol Vis Sci 2006; 47:3745-3753. [PMID:16936082]
22. Zolotukhin S, Potter M, Zolotukhin I, Sakai Y, Loiler S, Fraites TJ Jr, Chiodo VA, Phillipsberg T, Muzyczka N, Hauswirth WW, Flotte TR, Byrne BJ, Snyder RO. Production and purification of serotype 1, 2, and 5 recombinant adenoassociated viral vectors. Methods 2002; 28:158-167. [PMID:12413414]
23. Zolotukhin S, Byrne BJ, Mason E, Zolotukhin I, Potter M, Chesnut K, Summerford C, Samulski RJ, Muzyczka N. Recombinant adeno-associated virus purification using novel methods improves infectious titer and yield. Gene Ther 1999;6:973-985. [PMID: 10455399]
24. Jacobson SG, Acland GM, Aguirre GD, Aleman TS, Schwartz SB, Cideciyan AV, Zeiss CJ, Komaromy AM, Kaushal S, Roman AJ, Windsor EA, Sumaroka A, Pearce-Kelling SE, Conlon TJ, Chiodo VA, Boye SL, Flotte TR, Maguire AM, Bennett J, Hauswirth WW. Safety of Recombinant Adeno-Associated Virus Type 2-RPE65 Vector Delivered by Ocular Subretinal Injection. Mol Ther 2006; 13:1074-1084. [PMID:16644289]
25. Zeltner N, Kohlbrenner E, Clément N, Weber T, Linden RM. Near-perfect infectivity of wild-type AAV as benchmark for infectivity of recombinant AAV vectors. Gene Ther 2010; 17:872-879. [PMID: 20336156]
26. Pajusola K, Gruchala M, Joch H, Lüscher TF, Ylä-Herttuala S, Büeler H. Cell-Type Specific Characteristics Modulate the Transduction Efficiency of Adeno-Associated Virus Type 2 and Restrain Infection of Endothelial Cells. J Virol 2002; 76:11530-11540. [PMID: 12388714]
27. Zhu X, Ma B, Babu S, Murage J, Knox BE, Craft CM. Mouse cone arrestin gene characterization: promoter targets expression to cone photoreceptors. FEBS Lett 2002;524:116-122. [PMID: 12135752]
28. Flannery JG, Zolotukhin S, Vaquero MI, LaVail MM, Muzyczka N, Hauswirth WW. Efficient photoreceptortargeted gene expression in vivo by recombinant adenoassociated virus. Proc Natl Acad Sci USA 1997; 94:6916-6921. [PMID: 9192666]
29. Esumi N, Oshima Y, Li Y, Campochiaro PA, Zack DJ. Analysis of the VMD2 promoter and implication of E-box binding factors in its regulation. J Biol Chem 2004; 279:19064-9073. [PMID: 14982938]
30. Timmers AM, Zhang H, Squitieri A, Gonzalez-Pola C. Subretinal injections in rodent eyes: effects on electrophysiology and histology of rat retina. Mol Vis 2001; 7:131-137. [PMID: 11435999]
31. Petrs-Silva H, Dinculescu A, Li Q, Deng WT, Pang JJ, Min SH, Chiodo V, Neeley AW, Govindasamy L, Bennett A, Agbandje-McKenna M, Zhong L, Li B, Jayandharan GR, Srivastava A, Lewin AS, Hauswirth WW. Novel properties of tyrosine-mutant AAV2 vectors in the mouse retina. Mol Ther 2011; 19:293-301. [PMID: 21045809]
32. Boye SE, Boye SL, Hauswirth WW. Adeno associated Virus Gene Therapy in Mouse Models of Retinal Degeneration. Eye, Retina, and Visual System of the Mouse. Ch 50. Cambridge, MA: MIT Press; 2008. p. 605-619.
33. Auricchio A, Kobinger G, Anand V, Hildinger M, O'Connor E, Maguire AM, Wilson JM, Bennett J. Exchange of surface proteinsimpacts on viral vector cellular specificity and transduction characteristics: the retina as a model. Hum Mol Genet 2001; 10:3075-3081. [PMID: 11751689]
34. Sun X, Pawlyk B, Xu X, Liu X, Bulgakov OV, Adamian M, Sandberg MA, Khani SC, Tan MH, Smith AJ, Ali RR, Li T. Gene therapy with a promoter targeting both rods and cones rescues retinal degeneration caused by AIPL1 mutations. Gene Ther 2010; 17:117-131. [PMID: 19710705]
35. Tan MH, Smith AJ, Pawlyk B, Xu X, Liu X, Bainbridge JB, Basche M, McIntosh J, Tran HV, Nathwani A, Li T, Ali RR. 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. [PMID: 19299492]
36. Pawlyk BS, Bulgakov OV, Liu X, Xu X, Adamian M, Sun X, Khani SC, Berson EL, Sandberg MA, Li T. Replacement gene therapy with a human RPGRIP1 sequence slows photoreceptor degeneration in a murine model of leber congenital amaurosis. Hum Gene Ther 2010; 21:993-1004. [PMID: 20384479]
37. Park TK, Wu Z, Kjellstrom S, Zeng Y, Bush RA, Sieving PA, Colosi P. 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. [PMID:19458650]
38. Allocca M, Mussolino C, Garcia-Hoyos M, Sanges D, Iodice C, Petrillo M, Vandenberghe LH, Wilson JM, Marigo V, Surace EM, Auricchio A. Novel adeno-associated virus serotypes efficiently transduce murine photoreceptors. J Virol 2007; 81:11372-11380. [PMID: 17699581]
39. 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. [PMID: 18278824]
40. Lei B, Zhang K, Yue Y, Ghosh A, Duan D. Adeno-associated virus serotype-9 efficiently tranduces the retinal outer plexiform layer. Mol Vis 2009; 15:1374-1382. [PMID: 19626133]
41. Zhong L, Li B, Mah CS, Govindasamy L, Agbandje-McKenna M, Cooper M, Herzog RW, Zolotukhin I, Warrington KH Jr, Weigel-Van Aken KA, Hobbs JA, Zolotukhin S, Muzyczka N, Srivastava A. Next generation of adeno-associated virus 2 vectors: Point mutations in tyrosines lead to high-efficiency transduction at lower doses. Proc Natl Acad Sci USA 2008; 105:7827-7832. [PMID: 18511559]
42. Markusic DM, Herzog RW, Aslanidi GV, Hoffman BE, Li B, Li M, Jayandharan GR, Ling C, Zolotukhin I, Ma W, Zolotukhin S, Srivastava A, Zhong L. High-efficiency transduction and correction of murine hemophilia B using AAV2 vectors devoid of multiple surface-exposed tyrosines. Mol Ther 2010; 18:2048-2056. [PMID: 20736929]
43. Gao GP, Alvira MR, Wang L, Calcedo R, Johnston J, Wilson JM. Novel adeno-associated viruses from rhesus monkeys as vectors for human gene therapy. Proc Natl Acad Sci USA 2002; 99:11854-11859. [PMID: 12192090].12192090
44. Kauss MA, Smith LJ, Zhong L, Srivastava A, Wong KK Jr, Chatterjee S. Enhanced long-term transduction and multilineage engraftment of human hematopoietic stem cells transduced with tyrosine-modified recombinant adeno-associated virus serotype 2. Hum Gene Ther 2010; 21:1129-1136. [PMID: 20486772]
45. Dalkara D, Kolstad KD, Caporale N, Visel M, Klimczak RR, Schaffer DV, Flannery JG. Inner limiting membrane barriers to AAV-mediated retinal transduction from the vitreous. Mol Ther 2009; 17:2096-2102. [PMID: 19672248]
46. Hurlbut GD, Ziegler RJ, Nietupski JB, Foley JW, Woodworth LA, Meyers E, Bercury SD, Pande NN, Souza DW, Bree MP, Lukason MJ, Marshall J, Cheng SH, Scheule RK. Preexisting immunity and low expression in primates highlight translational challenges for liver-directed AAV8-mediated gene therapy. Mol Ther 2010; 18:1983-1994. [PMID:20736932]
47. Surace EM, Auricchio A, Reich SJ, Rex T, Glover E, Pineles S, Tang W, O'Connor E, Lyubarsky A, Savchenko A, Pugh EN Jr, Maguire AM, Wilson JM, Bennett J. Delivery of adenoassociated virus vectors to the fetal retina: impact of viral capsid proteins on the retinal neuronal progenitor transduction. J Virol 2003; 77:7957-7963. [PMID: 12829835]
48. Kolstad KD, Dalkara D, Guerin K, Visel M, Hoffmann N, Schaffer DV, Flannery JG. Changes in adeno-associated virus-mediated gene delivery in retinal degeneration. Hum Gene Ther 2010; 21:571-578. [PMID: 20021232]
49. Michalakis S, Mühlfriedel R, Tanimoto N, Krishnamoorthy V, Koch S, Fischer MD, Becirovic E, Bai L, Huber G, Beck SC, Fahl E, Büning H, Paquet-Durand F, Zong X, Gollisch T, Biel M, Seeliger MW. Restoration of cone vision in the CNGA3-/- mouse model of congenital complete lack of cone photoreceptor function. Mol Ther 2010; 18:2057-2063. [PMID: 20628362]
50. Le YZ, Zheng W, Rao PC, Zheng L, Anderson RE, Esumi N, Zack DJ, Zhu M. Inducible expression of cre recombinase in the retinal pigment epithelium. Invest Ophthalmol Vis Sci 2008; 49:1248-1253. [PMID: 18326755]