Adeno-associated virus (AAV) gene delivery in stem cell therapy

Discovery Medicine

Volumn 20, Issue 111, 2015, Pages 333-342

  Brown, Nolan J ^a   Hirsch, Matthew L ^b  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 6; LENTIVIRUS VECTOR; PARVOVIRUS VECTOR; PROTEIN P53; RETROVIRUS VECTOR;

APOPTOSIS; ARTICLE; CANCER CHEMOTHERAPY; CANCER RADIOTHERAPY; CLINICAL TRIAL (TOPIC); DNA DAMAGE; DRUG SAFETY; EMBRYONIC STEM CELL; GENE EXPRESSION; GENE MUTATION; GRAFT VERSUS HOST REACTION; HEMATOLOGIC DISEASE; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; NONHUMAN; STEM CELL TRANSPLANTATION; TOXICITY; TRANSGENE; VIRAL GENE THERAPY; BIOLOGICAL THERAPY; DEPENDOPARVOVIRUS; GENETIC DISEASES, INBORN; GENETIC TRANSDUCTION; GENETICS; HEMATOLOGIC DISEASES; HIV INFECTIONS; METABOLISM; PATHOLOGY; PROCEDURES; STEM CELL;

CELL- AND TISSUE-BASED THERAPY; DEPENDOVIRUS; GENETIC DISEASES, INBORN; HEMATOLOGIC DISEASES; HIV INFECTIONS; HUMANS; STEM CELLS; TRANSDUCTION, GENETIC;

EID: 84949759753     PISSN: 15396509     EISSN: 19447930     Source Type: Journal    
DOI: None     Document Type: Article

References (130)

1. Aldenhoven M, Wynr RF, Orchard PJ, O'Meara A, Veys P, Fischer A, Valayannopoulos V, Neven B, Rovelli A, Prasad VK, Tolar J, Allewelt H, Jones SA, Parini R, Renard M, Bordon V, Wulffraat NM, de Koning TJ, Shapiro EG, Kurtzberg J, et al. Long-term outcome of Hurler syndrome patients after hematopoietic cell transplantation: an international multicenter study. Blood 125:2164-2172, 2015.
2. Asahara T, Kalka C, Isner JM. Stem cell therapy and gene transfer for regeneration. Gene Ther 7:451-457, 2000.
3. Asokan A, Schaffer DV, Samulski RJ. The AAV vector toolkit: poised at the clinical crossroads. Mol Ther 20:699-708, 2012.
4. Asuri P, Bartel MA, Vazin T, Jang J-H, Wong TB, Schaffer DV. Directed evolution of adeno-associated virus for enhanced gene delivery and gene targeting in human pluripotent stem cells. Mol Ther 20:329-338, 2012.
5. Atchison RW, Casto BC, Hammon WM. Adenovirus-associated defective virus particles. Science 149:754-756, 1965.
6. Bartlett JS, Kleinschmidt J, Boucher RC, Samulski RJ. Targeted adeno-associated virus vector transduction of nonpermissive cells mediated by a bispecific F(ab'?)2 antibody. Nat Biotech 17:181-186, 1999.
7. Berns KI. Parvovirus replication. Microbiol Rev 54:316-329, 1990.
8. Berz D, McCormack EM, Winer ES, Colvin GA, Quesenberry PJ. Cryopreservation of hematopoietic stem cells. Am J Hematol 82:463-472, 2007.
9. Botquin V, Cid-Arregui A, Schlehofer JR. Adeno-associated virus type 2 interferes with early development of mouse embryos. J Gen Virol 75(Pt 10):2655-2662, 1994.
10. Bowles DE, McPhee SW, Li C, Gray SJ, Samulski JJ, Camp AS, Li J, Wang B, Monahan PE, Rabinowitz JE, Grieger JC, Govindasamy L, Agbandje-McKenna M, Xiao X, Samulski RJ. Phase 1 gene therapy for Duchenne muscular dystrophy using a translational optimized AAV vector. Mol Ther 20:443-455, 2012.
11. Calcedo R, Vandenberghe LH, Gao G, Lin J, Wilson JM. Worldwide epidemiology of neutralizing antibodies to adeno-associated viruses. J Infect Dis 199:381-390, 2009.
12. Cao L, During M, Xiao W. Replication competent helper functions for recombinant AAV vector generation. Gene Ther 9:1199-1206, 2002.
13. Cao A, Galanello R. Beta-thalassemia. Genet Med 12:61-76, 2010.
14. Cataldi MP, McCarty DM. Differential effects of DNA double-strand break repair pathways on single-strand and self-complementary adeno-associated virus vector genomes. J Virol 84:8673-8682, 2010.
15. Cataldi MP, McCarty DM. Hairpin end conformation of adeno-associated virus (AAV) genome determines interactions with DNA repair pathways. Gene Ther 20:686-693, 2013.
16. Cervelli T, Palacios JA, Zentilin L, Mano M, Schwartz RA, Weitzman MD, Giacca M. Processing of recombinant AAV genomes occurs in specific nuclear structures that overlap with foci of DNA-damage-response proteins. J Cell Sci 121:349-357, 2008.
17. Chatterjee S, Li W, Wong CA, Fisher-Adams G, Lu D, Guha M, Macer JA, Forman SJ, Wong KK. Transduction of primitive human marrow and cord blood-derived hematopoietic progenitor cells with adeno-associated virus vectors. Blood 93:1882-1894, 1999.
18. Chen S-J, Johnston J, Sandhu A, Bish LT, Hovhannisyan R, Jno-Charles O, Sweeney HL, Wilson JM. Enhancing the utility of adeno-associated virus gene transfer through inducible tissue-specific expression. Hum Gene Ther Methods 24:270-278, 2013.
19. Choi VW, Samulski RJ, McCarty DM. Effects of adeno-associated virus DNA hairpin structure on recombination. J Virol 79:6801-6807, 2005a.
20. Choi VW, McCarty DM, Samulski RJ. AAV hybrid serotypes: improved vectors for gene delivery. Curr Gene Ther 5:299-310, 2005b.
21. Choi VW, McCarty DM, Samulski RJ. Host cell DNA repair pathways in adeno-associated viral genome processing. J Virol 80:10346-10356, 2006.
22. Corbel SY, Lee A, Yi L, Duenas J, Brazelton TR, Blau HM, Rossi FMV. Contribution of hematopoietic stem cells to skeletal muscle. Nat Med 9:1528-1532, 2003.
23. Daya S, Berns KI. Gene therapy using adeno-associated virus vectors. Clin Microbiol Rev 21:583-593, 2008.
24. Deans AJ, West SC. FANCM connects the genome instability disorders Bloom's syndrome and Fanconi anemia. Molecular Cell 36:943-953, 2009.
25. Dravid G, Ye Z, Hammond H, Chen G, Pyle A, Donovan P, Yu X, Cheng L. Defining the role of Wnt/ß-catenin signaling in the survival, proliferation, and self-renewal of human embryonic stem cells. Stem Cells 23:1489-1501, 2005.
26. Dumitru R, Gama V, Fagan BM, Bower JJ, Swahari V, Pevny LH, Deshmukh M. Human embryonic stem cells have constitutively active Bax at the Golgi and are primed to undergo rapid apoptosis. Mol Cell 46:573-583, 2012.
27. Ellis BL, Hirsch ML, Barker JC, Connelly JP, Steininger RJ, Porteus MH. 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, 2013.
28. Evans M, Hunter S. Source and nature of embryonic stem cells. Comptes Rendus Biologies 325:1003-1007, 2002.
29. Ferrara JL, Levine JE, Reddy P, Holler E. Graft-versus-host disease. The Lancet 373:1550-1561, 2009.
30. Fisher-Adams G, Wong KJ, PodsakoffG, Forman SJ, Chatterjee S. Integration of adeno-associated virus vectors in CD34+ human hematopoietic progenitor cells after transduction. Blood 88:492-504, 1996.
31. Fragkos M, Beard P. Mitotic catastrophe occurs in the absence of apoptosis in p53-null cells with a defective G1 checkpoint. PLoS One 6:e22946, 2011.
32. Gao G, Vandenberghe L, Wilson J. New recombinant serotypes of AAV vectors. Curr Gene Ther 5:285-297, 2005.
33. Garner E, Martinon F, Tschopp J, Beard P, Raj K. Cells with defective p53-p21-pRb pathway are susceptible to apoptosis induced by p84N5 via caspase-6. Cancer Res 67:7631-7637, 2007.
34. Gonçalves MA. Adeno-associated virus: from defective virus to effective vector. Virol J 2:43, 2005.
35. Goodman S, Xiao X, Donahue RE, Moulton A, Miller J, Walsh C, Young NS, Samulski RJ, Nienhuis AW. Recombinant adeno-associated virus-mediated gene transfer into hematopoietic progenitor cells. Blood 84:1492-1500, 1994.
36. Grandela C, Pera MF, Wolvetang EJ. p53 is required for etoposide-induced apoptosis of human embryonic stem cells. Stem Cell Research 1:116-128, 2008.
37. Gray SJ, Blake BL, Criswell HE, Nicolson SC, Samulski RJ, McCown TJ. Directed evolution of a novel adeno-associated virus (AAV) vector that crosses the seizure-compromised blood-brain barrier (BBB). Mol Ther 18:570-578, 2010.
38. Grieger JC, Samulski RJ. Packaging capacity of adeno-associated virus serotypes: impact of larger genomes on infectivity and postentry steps. J Virol 79:9933-9944, 2005.
39. Griffith LM, Cowan MJ, Notarangelo LD, Puck JM, Buckley RH, Candotti F, Conley ME, Fleisher TA, Gaspar HB, Kohn DB, Ochs HD, O'Reilly RJ, Rizzo JD, Roifman CM, Small TN, Shearer WT. Improving cellular therapy for primary immune deficiency diseases: recognition, diagnosis, and management. J Allergy Clin Immunol 124:1152-1160, e12, 2009.
40. Gutierrez-Aranda I, Ramos-Mejia V, Bueno C, Munoz-Lopez M, Real PJ, Mácia A, Sanchez L, Ligero G, Garcia-Parez JL, Menendez P. Human induced pluripotent stem cells develop teratoma more efficiently and faster than human embryonic stem cells regardless the site of injection. Stem Cells 28:1568-1570, 2010.
41. Handa A, Muramatsu S, Qiu J, Mizukami H, Brown KE. Adeno-associated virus (AAV)-3-based vectors transduce haematopoietic cells not susceptible to transduction with AAV-2-based vectors. J Gen Virol 81:2077-2084, 2000.
42. Hansen J, Qing K, Kwon H-J, Mah C, Srivastava A. Impaired intracellular trafficking of adeno-associated virus type 2 vectors limits efficient transduction of murine fibroblasts. J Virol 74:992-996, 2000.
43. Haraguchi Y, Shimizu T, Yamato M, Okano T. Concise review: cell therapy and tissue engineering for cardiovascular disease. Stem Cells Trans Med 1:136-141, 2012.
44. Hargrove PW, Vanin EF, Kurtzman GJ, Nienhuis AW. High-level globin gene expression mediated by a recombinant adeno-associated virus genome that contains the 3' ? globin gene regulatory element and integrates as tandem copies in erythroid cells. Blood 89:2167-2175, 1997.
45. Henckaerts E, Dutheil N, Zeltner N, Kattman S, Kohlbrenner E, Ward P, Clément N, Rebollo P, Kennedy M, Keller GM, Linden RM. Site-specific integration of adeno-associated virus involves partial duplication of the target locus. Proc Natl Acad Sci U S A 106:7571-7576, 2009.
46. Hess DC, Abe T, Hill WD, Studdard AM, Carothers J, Masuya M, Fleming PA, Drake CJ, Ogawa M. Hematopoietic origin of microglial and perivascular cells in brain. Exp Neurol 186:134-144, 2004.
47. Hewitt FC, Li C, Gray SJ, Cockrell S, Washburn M, Samulski RJ. Reducing the risk of adeno-associated virus (AAV) vector mobilization with AAV type 5 vectors. J Virol 83:3919-3929, 2009.
48. Hirsch ML, Storici F, Li C, Choi VW, Samulski RJ. AAV recombineering with single strand oligonucleotides. PLoS One 4:e7705 2009.
49. Hirsch ML, Agbandje-McKenna M, Jude Samulski R. Little vector, big gene transduction: fragmented genome reassembly of adeno-associated virus. Mol Ther 18:6-8, 2010.
50. Hirsch ML, Fagan BM, Dumitru R, Bower JJ, Yadav S, Porteus MH, Pevny LH, Samulski RJ. Viral single-strand DNA induces p53-dependent apoptosis in human embryonic stem cells. PLoS One 6:e27520, 2011.
51. Hirsch ML, Li C, Bellon I, Yin C, Chavala S, Pryadkina M, Richard I, Samulski RJ. Oversized AAV transduction is mediated via a DNA-PKcs-independent, Rad51C-dependent repair pathway. Mol Ther 21:2205-2216, 2013.
52. Hirsch M. Adeno-associated virus inverted terminal repeats stimulate gene editing. Gene Ther 22:190-195, 2015.
53. Holkers M, de Vries AAF, Gonçalves MAFV. Nonspaced inverted DNA repeats are preferential targets for homology-directed gene repair in mammalian cells. Nucleic Acids Res 40:1984-1999, 2012.
54. Holt N, Wang J, Kim K, Friedman G, Wang X, Taupin V, Crooks GM, Kohn DB, Gregory PD, Holmes MC, Cannon PM. Human hematopoietic stem/progenitor cells modified by zinc-finger nucleases targeted to CCR5 control HIV-1 in vivo. Nat Biotechnol 28:839-847, 2010.
55. Hou P, Li Y, Zhang X, Liu C, Guan J, Li H, Zhao T, Ye J, Yang W, Liu K, Ge J, Xu J, Zhang Q, Zhao Y, Deng H. Pluripotent stem cells induced from mouse somatic cells by small-molecule compounds. Science 341:651-654, 2013.
56. Inagaki K, Ma C, Storm TA, Kay MA, Nakai H. The role of DNA-PKcs and Artemis in opening viral DNA hairpin termini in various tissues in mice. J Virol 81:11304-11321, 2007.
57. Ingemarsdotter C, Keller D, Beard P. The DNA damage response to non-replicating adeno-associated virus: centriole overduplication and mitotic catastrophe independent of the spindle checkpoint. Virology 400:271-286, 2010.
58. Jiang Y, Jahagirdar BN, Reinhardt RL, Schwartz RE, Keene CD, Ortiz-Gonzalez XR, Reyes M, Lenvik T, Lund T, Blackstad M, Du J, Aldrich S, Lisberg A, Low WC, Largaespada DA, Verfaillie CM. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418:41-49, 2002.
59. Jang J-H, Koerber JT, Kim J-S, Asuri P, Vazin T, Bartel M, Keung A, Kwon I, Park KI, Schaffer DV. An evolved adeno-associated viral variant enhances gene delivery and gene targeting in neural stem cells. Mol Ther 19:667-675, 2011.
60. Jurvansuu J, Fragkos M, Ingemarsdotter C, Beard P. Chk1 instability is coupled to mitotic cell death of p53-deficient cells in response to virus-induced DNA damage signaling. J Mol Biol 372:397-406, 2007.
61. Kang Y, Liao W, Yuan Z, Sheng P, Zhang L, Yuan X, Lei L. In vitro and in vivo induction of bone formation based on adeno-associated virus-mediated BMP-7 gene therapy using human adipose-derived mesenchymal stem cells. Acta Pharmacol Sin 28:839-849, 2007.
62. Khan IF, Hirata RK, Wang P-R, Li Y, Kho J, Nelson A, Huo Y, Zavaljevski M, Ware C, Russell DW. Engineering of human pluripotent stem cells by AAV-mediated gene targeting. Mol Ther 18:1192-1199, 2010.
63. Kiem H-P, Jerome KR, Deeks SG, McCune JM. Hematopoietic-stem-cell-based gene therapy for HIV disease. Cell Stem Cell 10:137-147, 2012.
64. Kim JH, Park S-N, Suh H. Generation of insulin-producing human mesenchymal stem cells using recombinant adeno-associated virus. Yonsei Med J 48:109-119, 2007.
65. Körbling M. Peripheral blood stem cells: a novel source for allogeneic transplantation. The Oncologist 2:104-104, 1997.
66. Laface D, Hermonat P, Wakeland E, Peck A. Gene transfer into hematopoietic progenitor cells mediated by an adeno-associated virus vector. Virol J 162:483-486, 1988.
67. Lagasse E, Connors H, Al-Dhalimy M, Reitsma M, Dohse M, Osborne L, Wang X, Finegold M, Weissman IL, Grompe M. Purified hematopoietic stem cells can differentiate into hepatocytes in vivo. Nat Med 6:1229-1234, 2000.
68. Li C, Narkbunnam N, Samulski RJ, Asokan A, Hu G, Jacobson LJ, Manco-johnson MJ, Monahan PE. Neutralizing antibodies against adeno-associated virus examined prospectively in pediatric patients with hemophilia. Gene Ther 19:288-94, 2012.
69. Lim WF, Inoue-Yokoo T, Tan KS, Lai MI, Sugiyama D. Hematopoietic cell differentiation from embryonic and induced pluripotent stem cells. Stem Cell Res Ther 4:71, 2013.
70. Lindvall O, Kokaia Z, Martinez-Serrano A. Stem cell therapy for human neurodegenerative disorders-how to make it work. Nat Med 10:S42-S50, 2004.
71. Liu X, Li J, Hu C, Zhou Q, Zhang W, Hu M, Zhou J, Wang J. Significant expansion of the fluorescent protein chromophore through the genetic incorporation of a metal-chelating unnatural amino acid. Angew Chem Int Ed 52:4805-4809, 2013.
72. Ma S, Xie N, Li W, Yuan B, Shi Y, Wang Y. Immunobiology of mesenchymal stem cells. Cell Death Differ 21:216-225, 2014.
73. Mackie AR, Losordo DW. CD34-positive stem cells in the treatment of heart and vascular disease in human beings. Tex Heart Inst J 38:474-485, 2011.
74. Malik P, McQuiston SA, Yu XJ, Pepper KA, Krall WJ, PodsakoffGM, Kurtzman GJ, Kohn DB. Recombinant adeno-associated virus mediates a high level of gene transfer but less efficient integration in the K562 human hematopoietic cell line. J Virol 71:1776-1783, 1997.
75. Mano M, Ippodrino R, Zentilin L, Zacchigna S, Giacca M. Genome-wide RNAi screening identifies host restriction factors critical for in vivo AAV transduction. PNAS 112:11276-11281, 2015.
76. Martello G, Smith A. The nature of embryonic stem cells. Annu Rev Cell Develop Biol 30:647-675, 2014.
77. McCarty DM, Monahan PE, Samulski RJ. Self-complementary recombinant adeno-associated virus (scAAV) vectors promote efficient transduction independently of DNA synthesis. Gene Ther 8:1248-1254, 2001.
78. Miller JL, Donahue RE, Sellers SE, Samulski RJ, Young NS, Nienhuis AW. Recombinant adeno-associated virus (rAAV)-mediated expression of a human gamma-globin gene in human progenitor-derived erythroid cells. Proc Natl Acad Sci U S A 91:10183-10187, 1994.
79. Mingozzi F, High KA. Therapeutic in vivo gene transfer for genetic disease using AAV: progress and challenges. Nat Rev Genet 12:341-55, 2011.
80. Mitsui K, Suzuki K, Aizawa E, Kawase E, Suemori H, Nakatsuji N, Mitani K. Gene targeting in human pluripotent stem cells with adeno-associated virus vectors. Biochem Biophys Res Comm 388:711-717, 2009.
81. Momcilovic O, Knobloch L, Fornsaglio J, Varum S, Easley C, Schatten G. DNA damage responses in human induced pluripotent stem cells and embryonic stem cells. PLoS One 5:e13410, 2010.
82. Nadig RR. Stem cell therapy - hype or hope? A review. J Conserv Dent 12:131-138, 2009.
83. Nathwani AC, Hanawa H, VandergriffJ, Kelly P, Vanin EF, Nienhuis AW. Efficient gene transfer into human cord blood CD34+ cells and the CD34+CD38-subset using highly purified recombinant adeno-associated viral vector preparations that are free of helper virus and wild-type AAV. Gene Ther 7:183-95, 2000.
84. Okano H, Nakamura M, Yoshida K, Okada Y, Tsuji O, Nori S, Ikeda E, Yamanaka S, Miura K. Steps toward safe cell therapy using induced pluripotent stem cells. Circ Res 112:523-533, 2013.
85. Otsu M. Perspectives on stem cell gene therapy for genetic disorders. VOXS 10:231-234, 2015.
86. Penaud-Budloo M, Le Guiner C, Nowrouzi A, ToromanoffA, Chérel Y, Chenuaud P, Schmidt M, von Kalle C, Rolling F, Moullier P, Snyder RO. Adeno-associated virus vector genomes persist as episomal chromatin in primate muscle. J Virol 82:7875-7885, 2008.
87. Phillips JL, Hegge J, WolffJA, Samulski RJ, Asokan A. Systemic gene transfer to skeletal muscle using reengineered AAV vectors. Methods Mol Biol 709:141-151, 2011.
88. Pluchino S, Quattrini A, Brambilla E, Gritti A, Salani G, Dina G, Galli R, Del Carro U, Amadio S, Bergami A, Furlan R, Comi G, Vescovi AL, Martino G. Injection of adult neurospheres induces recovery in a chronic model of multiple sclerosis. Nature 422:688-694, 2003.
89. Ponnazhagan S, Mukherjee P, Wang XS, Qing K, Kube DM, Mah C, Kurpad C, Yoder MC, Srour EF, Srivastava A. Adeno-associated virus type 2-mediated transduction in primary human bone marrow-derived CD34+ hematopoietic progenitor cells: donor variation and correlation of transgene expression with cellular differentiation. J Virol 71:8262-8267, 1997.
90. Ponnazhagan S, Wang X-S, Woody MJ, Luo F, Kang LY, Nallari ML, Munshi NC, Zhou SZ, Srivastava A. Differential expression in human cells from the p6 promoter of human parvovirus B19 following plasmid transfection and recombinant adeno-associated virus 2 (AAV) infection: human megakaryocytic leukaemia cells are non-permissive for AAV infection. J Gen Virol 77:1111-1122, 1996.
91. Ponnazhagan S, Yoder MC, Srivastava A. Adeno-associated virus type 2-mediated transduction of murine hematopoietic cells with long-term repopulating ability and sustained expression of a human globin gene in vivo. J Virol 71:3098-3104, 1997.
92. Pulicherla N, Shen S, Yadav S, Debbink K, Govindasamy L, Agbandje-McKenna M, Asokan A. Engineering liver-detargeted AAV9 vectors for cardiac and musculoskeletal gene transfer. Mol Ther 19:1070-1078, 2011.
93. Qing K, Khuntirat B, Mah C, Kube DM, Wang XS, Ponnazhagan S, Zhou S, Dwarki VJ, Yoder MC, Srivastava A. Adeno-associated virus type 2-mediated gene transfer: correlation of tyrosine phosphorylation of the cellular single-stranded D sequence-binding protein with transgene expression in human cells in vitro and murine tissues in vivo. J Virol 72:1593-1599, 1998.
94. Raj K, Ogston P, Beard P. Virus-mediated killing of cells that lack p53 activity. Nature 412:914-917, 2001.
95. Rapti K, Stillitano F, Karakikes I, Nonnenmacher M, Weber T, Hulot J-S, Hajjar RJ. Effectiveness of gene delivery systems for pluripotent and differentiated cells. Mol Ther Methods Clin Dev 2:14067, 2015.
96. Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature 414:105-111, 2001.
97. Rutledge EA, Russell DW. Adeno-associated virus vector integration junctions. J Virol 71:8429-8436, 1997.
98. Samulski RJ, Berns KI, Tan M, Muzyczka N. Cloning of adeno-associated virus into pBR322: rescue of intact virus from the recombinant plasmid in human cells. Proc Natl Acad Sci U S A 79:2077-2081, 1982.
99. Samulski RJ, Muzyczka N. AAV-mediated gene therapy for research and therapeutic purposes. Annu Rev Virol 1:427-451, 2014.
100. Schimmenti S, Boesen J, Claassen EA, Valerio D, Einerhand MP. Long-term genetic modification of rhesus monkey hematopoietic cells following transplantation of adeno-associated virus vector-transduced CD34+ cells. Hum Gene Ther 9:2727-2734, 1998.
101. Schwartz RA, Palacios JA, Cassell GD, Adam S, Giacca M, Weitzman MD. The Mre11/Rad50/Nbs1 complex limits adeno-associated virus transduction and replication. J Virol 81:12936-12945, 2007.
102. Schwartz RA, Carson CT, Schuberth C, Weitzman MD. Adeno-associated virus replication induces a DNA damage response coordinated by DNA-dependent protein kinase. J Virol 83:6269-6278, 2009.
103. Shen S, Horowitz ED, Troupes AN, Brown SM, Pulicherla N, Samulski RJ, Agbandje-McKenna M, Asokan A. Engraftment of a galactose receptor footprint onto adeno-associated viral capsids improves transduction efficiency. J Biol Chem 288:28814-28823, 2013.
104. Smith-Arica JR, Thomson AJ, Ansell R, Chiorini J, Davidson B, McWhir J. Infection efficiency of human and mouse embryonic stem cells using adenoviral and adeno-associated viral vectors. Cloning Stem Cells 5:51-62, 2003.
105. Song L, Kauss MA, Kopin E, Chandra M, Ul-Hasan T, Miller E, Jayandharan GR, Rivers AE, Aslanidi GV, Ling C, Li B, Ma W, Li X, Andino LM, Zhong L, Tarantal AF, Yoder MC, Wong KK, Tan M, Chatterjee S, et al. Optimizing the transduction efficiency of human hematopoietic stem cells using capsid-modified AAV6 vectors in vitro and in a xenograft mouse model in vivo. Cytotherapy 15:986-998, 2013.
106. Sonntag F, Schmidt K, Kleinschmidt JA. A viral assembly factor promotes AAV2 capsid formation in the nucleolus. Proc Natl Acad Sci U S A 107:10220-10225, 2010.
107. Srivastava A. Hematopoietic stem cell transduction by recombinant adeno-associated virus vectors: problems and solutions. Hum Gene Ther 16:792-798, 2005.
108. Stary J, Locatelli F, Niemeyer CM. Stem cell transplantation for aplastic anemia and myelodysplastic syndrome. Bone Marrow Transplant 35:S13-S16, 2005.
109. Stender S, Murphy M, O'Brien T, Stengaard C, Ulrich-Vinther M, Søballe K, Barry F. Adeno-associated viral vector transduction of human mesenchymal stem cells. Eur Cell Mater 13:93-99; discussion 99, 2007.
110. Stilwell JL, Samulski RJ. Role of viral vectors and virion shells in cellular gene expression. Mol Ther 9:337-346, 2004.
111. Taghizadeh RR, Cetrulo KJ, Cetrulo CL. Wharton's jelly stem cells: future clinical applications. Placenta 32(Suppl 4):S311-S315, 2011.
112. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663-676, 2006.
113. Tan M, Qing K, Zhou S, Yoder MC, Srivastava A. Adeno-associated virus 2-mediated transduction and erythroid lineage-restricted long-term expression of the human ß-globin gene in hematopoietic cells from homozygous ß-thalassemic mice. Mol Ther 3:940-946, 2001.
114. Tasher D, Dalal I. The genetic basis of severe combined immunodeficiency and its variants. Appl Clin Genet 5:67-80, 2012.
115. Tenenbaum L, Lehtonen E, Monahan PE. Evaluation of risks related to the use of adeno-associated virus-based vectors. Curr Gene Ther 3:545-565, 2003.
116. Tobiasch E, Rabreau M, Geletneky K, Laruë-Charlus S, Severin F, Becker N, Schlehofer JR. Detection of adeno-associated virus DNA in human genital tissue and in material from spontaneous abortion. J Med Virol 44:215-222, 1994.
117. van Os R, Avraham H, Banu N, Mauch PM, Whater J, Yang Y, Du B. Recombinant adeno-associated virus-based vectors provide short-term rather than long-term transduction of primitive hematopoietic stem cells. Stem Cells 17:117-120, 1999.
118. Verlinsky Y, Strelchenko N, Kukharenko V, Rechitsky S, Verlinsky O, Galat V, Kuliev A. Human embryonic stem cell lines with genetic disorders. Reproductive BioMedicine Online 10:105-110, 2005.
119. Walsh CE, Nienhuis AW, Samulski RJ, Brown MG, Miller JL, Young NS, Liu JM. Phenotypic correction of Fanconi anemia in human hematopoietic cells with a recombinant adeno-associated virus vector. J Clin Invest 94:1440-1448, 1994.
120. Wang Z, Ma H-I, Li J, Sun L, Zhang J, Xiao X. Rapid and highly efficient transduction by double-stranded adeno-associated virus vectors in vitro and in vivo. Gene Ther 10:2105-2111, 2003.
121. Wang M, Crosby A, Hastie E, Samulski JJ, McPhee S, Joshua G, Samulski RJ, Li C. Prediction of adeno-associated virus neutralizing antibody activity for clinical application. Gene Ther, doi:10.1038/gt.2015.69, 2015.
122. Weitzman MD, Kyöstiö SR, Kotin RM, Owens RA. Adeno-associated virus (AAV) Rep proteins mediate complex formation between AAV DNA and its integration site in human DNA. Proc Natl Acad Sci U S A 91:5808-5812, 1994.
123. Wu Z, Yang H, Colosi P. Effect of genome size on AAV vector packaging. Mol Ther 18:80-86, 2009.
124. Xie Q, Bu W, Bhatia S, Hare J, Somasundaram T, Azzi A, Chapman MS. The atomic structure of adeno-associated virus (AAV-2), a vector for human gene therapy. PNAS 99:10405-10410, 2002.
125. Xiao X, Li J, Samulski RJ. Efficient long-term gene transfer into muscle tissue of immunocompetent mice by adeno-associated virus vector. J Virol 70:8098-8108, 1996.
126. Yang Q, Mamounas M, Yu G, Kennedy S, Leaker B, Merson J, Wong-Staal F, Yu M, Barber JR. Development of novel cell surface CD34-targeted recombinant adeno-associated virus vectors for gene therapy. Hum Gene Ther 9:1929-1937, 1998.
127. Zhong L, Li W, Li Y, Zhao W, Wu J, Li B, Maina N, Bischof D, Qing K, Weigel-Kelley KA, Zolotukhin I, Warrington KH, Li X, Slayton WB, Yoder MC, Srivastava A. Evaluation of primitive murine hematopoietic stem and progenitor cell transduction in vitro and in vivo by recombinant adeno-associated virus vector serotypes 1 through 5. Hum Gene Ther 17:321-333, 2006.
128. Zincarelli C, Soltys S, Rengo G, Rabinowitz JE. Analysis of AAV serotypes 1-9 mediated gene expression and tropism in mice after systemic injection. Mol Ther 16:1073-1080, 2008.
129. Zinn E, Pacouret S, Khaychuk V, Turunen HT, Carvalho LS, Andres-Mateos E, Shah S, Shelke R, Maurer AC, Plovie E, Xiao R, Vandenberghe LH. In silico reconstruction of the viral evolutionary lineage yields a potent gene therapy vector. Cell Rep 12:1056-1068, 2015.
130. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucl Acids Res 31:3406-3415, 2003.