Integration of adeno-associated virus (AAV) and recombinant AAV vectors

Annual Review of Genetics

Volumn 38, Issue , 2004, Pages 819-845

  McCarty, Douglas M ^a,b   Young Jr , Samuel M ^c   Samulski, R Jude ^b  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

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

^c SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

AAV; Gene therapy; Integration; Site specific; Vector

Indexed keywords

PARVOVIRUS VECTOR;

ADENO ASSOCIATED VIRUS; CHROMOSOME 19; DNA STRAND BREAKAGE; EPISOME; GENE DISRUPTION; HOST CELL; HUMAN; INFECTION; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROGENY; PROVIRUS; REVIEW; RISK ASSESSMENT; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY; VIRUS GENOME;

CELL LINE; CHROMOSOMES, HUMAN, PAIR 19; DEPENDOVIRUS; DNA; GENE THERAPY; GENETIC VECTORS; GENOME, VIRAL; HELA CELLS; HUMANS; RECOMBINATION, GENETIC; VIRUS INTEGRATION;

ADENO-ASSOCIATED VIRUS; DNA VIRUSES; PARVOVIRUS;

EID: 10944269753     PISSN: 00664197     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.genet.37.110801.143717     Document Type: Review

References (111)

1. Allen C, Miller CA, Nickoloff JA. 2003. The mutagenic potential of a single DNA double-strand break in a mammalian chromosome is not influenced by transcription. DNA Repair 2:1147-56
2. Amiss TJ, McCarry DM, Skulimowski A, Samulski RJ. 2003. Identification and characterization of an adeno-associated virus integration site in CV-1 cells from the African green monkey. J. Virol. 77:1904-15
3. Bakowska JC, Di Maria MV, Camp SM, Wang Y, Allen PD, Breakefield XO. 2003. Targeted transgene integration into transgenic mouse fibroblasts carrying the full-length human AAVS1 locus mediated by HSV/AAV rep(+) hybrid amplicon vector. Gene Ther. 10:1691-702
4. Balague C, Kalla M, Zhang WW. 1997. Adeno-associated virus Rep78 protein and terminal repeats enhance integration of DNA sequences into the cellular genome. J. Virol. 71:3299-306
5. Batchu RB, Hermonat PL. 1995. The trans-inhibitory Rep78 protein of adeno-associated virus binds to TAR region DNA of the human immunodeficiency virus type 1 long terminal repeat. FEBS Lett. 367:267-71
6. Berns KI, Cheung A, Ostrove J, Lewis M. 1982. Adeno-associated virus latent infection. In Virus Persistance, ed. BWJ Mahy, AC Minson, GK Darby, pp. 249-65. Cambridge: Cambridge Univ. Press
7. Brister JR, Muzyczka N. 2000. Mechanism of Rep-mediated adeno-associated virus origin nicking. J. Virol. 74:7762-71
8. Chang L-S, Shenk T. 1990. The adenovirus DNA binding protein stimulates the rate of transcription directed by adenovirus and adeno-associated virus promoters. J. Virol. 64:2103-9
9. Chang L-S, Shi Y, Shenk T. 1989. Adeno-associated virus p5 promoter contains an adenovirus EIA inducible element and a binding site for the major late transcription factor. J. Virol. 63:3479-88
10. Cheung AK, Hoggan MD, Hauswirth WW, Berns KI. 1980. Integration of the adeno-associated virus genome into cellular DNA in latently infected human Detroit 6 cells. J. Virol. 33:739-48
11. Chiorini JA, Yang L, Safer B, Kotin RM. 1995. Determination of adeno-associated virus Rep68 and Rep78 binding sites by random sequence oligonucleotide selection. J. Virol. 69:7334-38
12. Duan D, Sharma P, Yang J, Yue Y, Dudus L, et al. 1998. Circular intermediates of recombinant adeno-associated virus have defined structural characteristics responsible for long-term episomal persistence in muscle tissue. J. Virol. 72:8568-77. Erratum. 1999. J. Virol. 73(1):861
13. Duan D, Sharma P, Yang J, Yue Y, Dudus L, et al. 1998. Circular intermediates of recombinant adeno-associated virus have defined structural characteristics responsible for long-term episomal persistence in muscle tissue. J. Virol. 72:8568-77. Erratum. 1999. J. Virol. 73(1):861
14. Duan D, Yan Z, Yue Y, Engelhardt JF. 1999. Structural analysis of adeno-associated virus transduction circular intermediates. Virology 261:8-14
15. Dutheil N, Shi F, Dupressoir T, Linden RM. 2000. Adeno-associated virus site-specifically integrates into a muscle-specific DNA region. Proc. Natl. Acad. Sci. USA 97:4862-66
16. Dyall J, Szabo P, Berns KI. 1999. Adeno-associated virus (AAV) site-specific integration: formation of AAV-AAVS1 junctions in an in vitro system. Proc. Natl. Acad. Sci. USA 96:12849-54
17. Fisher KJ, Jooss K, Alston J, Yang Y, Haecker SE, et al. 1997. Recombinant adeno-associated virus for muscle directed gene therapy. Nat. Med. 3:306-12
18. Rotte TR, Afione SA, Solow R, Drumm ML, Markakis D, et al. 1993. Expression of the cystic fibrosis transmembrane conductance regulator from a novel adeno-associated virus promoter. J. Biol. Chem. 268:3781-90
19. Flotte TR, Afione SA, Zeitlin PL. 1994. Adeno-associated virus vector gene expression occurs in nondividing cells in the absence of vector DNA integration. Am. J. Respir. Cell Mol. Biol. 11:517-21
20. Giraud C, Winocour E, Berns KI. 1994. Site-specific integration by adeno-associated virus is directed by a cellular DNA sequence. Proc. Natl. Acad. Sci. USA 91:10039-43
21. Giraud C, Winocour E, Berns KI. 1995. Recombinant junctions formed by site-specific integration of adeno-associated virus into an episome. J. Virol. 69:6917-24
22. Haberman RP, McCown TJ, Samulski RJ. 2000. Novel transcriptional regulatory signals in the adeno-associated virus terminal repeat A/D junction element. J. Virol. 74:8732-39
23. Hacein-Bey-Abina S, Von Kalle C, Schmidt M, McCormack MP, Wulffraat N, et al. 2003. LMO2-associated clonal T cell proliferation in two patients after gene therapy for SCID-X1. Science 302:415-19
24. Harui A, Suzuki S, Kochanek S, Mitani K. 1999. Frequency and stability of chromosomal integration of adenovirus vectors. J. Virol. 73:6141-46
25. Hermonat PL, Muzyczka N. 1984. Use of adeno-associated virus as a mammalian DNA cloning vector: transduction of neomycin resistance into mammalian tissue culture cells. Proc. Natl. Acad. Sci. USA 81:6466-70
26. Hernandez YJ, Wang J, Kearns WG, Loiler S, Poirier A, Flotte TR. 1999. Latent adeno-associated virus infection elicits humoral but not cell-mediated immune responses in a nonhuman primate model. J. Virol. 73:8549-58
27. Hoggan MD. 1970. Adeno-associated viruses. Prog. Med. Virol. 12:211-39
28. Hoggan MD, Blacklow NR, Rowe WP. 1966. Studies of small DNA viruses found in various adenovirus preparations: physical, biological, and immunological characteristics. Proc. Natl. Acad. Sci. USA 55:1457-71
29. th, Cocoyac, Mexico
30. Huser D, Heilbronn R. 2003. Adeno-associated virus integrates site-specifically into human chromosome 19 in either orientation and with equal kinetics and frequency. J. Gen. Virol. 84:133-37
31. Huser D, Weger S, Heilbronn R. 2002. Kinetics and frequency of adeno-associated virus site-specific integration into human chromosome 19 monitored by quantitative real-time PCR. J. Virol. 76:7554-59
32. Huttner NA, Girod A, Schnittger S, Schoch C, Hallek M, Buning H. 2003. Analysis of site-specific transgene integration following cotransduction with recombinant adeno-associated virus and a rep encoding plasmid. J. Gene Med. 5:120-29
33. Im D-S, Muzyczka N. 1989. Factors that bind to the AAV terminal repeats. J. Virol. 63:3095-104
34. Im D-S, Muzyczka N. 1990. The AAV origin binding protein Rep68 is an ATP-dependent site-specific endonuclease with DNA helicase activity. Cell 61:447-57
35. Inoue N, Dong R, Hirata RK, Russell DW. 2001. Introduction of single base substitutions at homologous chromosomal sequences by adeno-associated virus vectors. Mol. Ther. 3:526-30
36. Inoue N, Hirata RK, Russell DW. 1999. High-fidelity correction of mutations at multiple chromosomal positions by adeno-associated virus vectors. J. Virol. 73:7376-80
37. Johnston KM, Jacoby D, Pechan PA, Fraefel C, Borghesani P, et al. 1997. HSV/AAV hybrid amplicon vectors extend transgene expression in human glioma cells. Hum. Gene Ther. 8:359-70
38. Kearns WG, Afione SA, Fulmer SB, Pang MC, Erikson D, et al. 1996. Recombinant adeno-associated virus (AAV-CFTR) vectors do not integrate in a site-specific fashion in an immortalized epithelial cell line. Gene Ther. 3:748-55
39. Kogure K, Urabe M, Mizukami H, Kume A, Sato Y, et al. 2001. Targeted integration of foreign DNA into a defined locus on chromosome 19 in K562 cells using AAV-derived components. Int. J. Hematol. 73:469-75
40. Kokorina NA, Santin AD, Li C, Hermonat PL. 1998. Involvement of protein-DNA interaction in adeno-associated virus Rep78-mediated inhibition of HIV-1. J. Hum. Virol. 1:441-50
41. Kotin RM, Berns KI. 1989. Organization of adeno-associated virus DNA in latently infected Detroit 6 cells. Virology 170:460-67
42. Kotin RM, Linden RM, Berns KI. 1992. Characterization of a preferred site on human chromosome 19q for integration of adeno-associated virus DNA by nonhomologous recombination. EMBO J. 11:5071-78
43. Kotin RM, Siniscalco M, Samulski RJ, Zhu XD, Hunter L, et al. 1990. Site-specific integration by adeno-associated virus. Proc. Natl. Acad. Sci. USA 87:2211-15
44. Lackner DF, Muzyczka N. 2002. Studies of the mechanism of transactivation of the adeno-associated virus p19 promoter by Rep protein. J. Virol. 76:8225-35
45. Lam P, Hui KM, Wang Y, Allen PD, Louis DN, et al. 2002. Dynamics of transgene expression in human glioblastoma cells mediated by herpes simplex virus/adeno-associated virus amplicon vectors. Hum. Gene Ther. 13:2147-59
46. Lamartina S, Roscilli G, Rinaudo D, Delmastro P, Toniatti C. 1998. Lipofection of purified adeno-associated virus Rep68 protein: toward a chromosome-targeting nonviral particle. J. Virol. 72:7653-58
47. Lamartina S, Sporeno E, Fattori E, Toniatti C. 2000. Characteristics of the adeno-associated virus preintegration site in human chromosome 19: open chromatin conformation and transcription-competent environment. J. Virol. 74:7671-77
48. Linden RM, Ward P, Giraud C, Winocour E, Berns KI. 1996. Site-specific integration by adeno-associated virus. Proc. Natl. Acad. Sci. USA 93:11288-94
49. Linden RM, Winocour E, Berns KI. 1996. The recombination signals for adeno-associated virus site-specific integration. Proc. Natl. Acad. Sci. USA 93:7966-72
50. McCarty DM, Pereira DJ, Zolotukhin I, Zhou X, Ryan JH, Muzyczka N. 1994. Identification of linear DNA sequences that specifically bind the adeno-associated virus Rep protein. J. Virol. 68:4988-97
51. McCarty DM, Ryan JH, Zolotukhin S, Zhou X, Muzyczka N. 1994. Interaction of the adeno-associated virus Rep protein with a sequence within the A palindrome of the viral terminal repeat. J. Virol. 68:4998-5006
52. McCarty DM, Samulski RJ. 1997. Adeno-associated viral vectors. In Concepts in Gene Therapy, ed. M Strauss, JA Barranger, pp. 61-78. Berlin: Walter de Gruyter
53. McLaughlin SK, Collis P, Hermonat PL, Muzyczka N. 1988. Adeno-associated virus general transduction vectors: analysis of proviral structures. J. Virol. 62:1963-73
54. Mendelson E, Miller IL, Carter BJ. 1988. Expression and rescue of a nonselected marker from an integrated AAV vector. Virology 166:154-65
55. Mendelson E, Smith MG, Miller IL, Carter BJ. 1988. Effect of a viral rep gene on transformation of cells by an adeno-associated virus vector. Virology 166:612-15
56. Miao CH, Nakai H, Thompson AR, Storm TA, Chiu W, et al. 2000. Nonrandom transduction of recombinant adeno-associated virus vectors in mouse hepatocytes in vivo: Cell cycling does not influence hepatocyte transduction. J. Virol. 74:3793-803
57. Miao CH, Snyder RO, Schowalter DB, Patijn GA, Donahue B, et al. 1998. The kinetics of rAAV integration in the liver [letter]. Nat. Genet. 19:13-15
58. Miller DG, Petek LM, Russell DW. 2004. Adeno-associated virus vectors integrate at chromosome breakage sites. Nat. Genet. 36:767-73
59. Miller DG, Rutledge EA, Russell DW. 2002. Chromosomal effects of adeno-associated virus vector integration. Nat. Genet. 30:147-48
60. Nakai H, Iwaki Y, Kay MA, Couto LB. 1999. Isolation of recombinant adeno-associated virus vector-cellular DNA junctions from mouse liver. J. Virol. 73:5438-47
61. Nakai H, Montini E, Fuess S, Storm TA, Grompe M, Kay MA. 2003. AAV serotype 2 vectors preferentially integrate into active genes in mice. Nat. Genet. 34:297-302
62. Nakai H, Montini E, Fuess S, Storm TA, Meuse L, et al. 2003. Helper-independent and AAV-ITR-independent chromosomal integration of double-stranded linear DNA vectors in mice. Mol. Ther. 7:101-11
63. Nakai H, Storm TA, Kay MA. 2000. Recruitment of single-stranded recombinant adeno-associated virus vector genomes and intermolecular recombination are responsible for stable transduction of liver in vivo. J. Virol. 74:9451-63
64. Nakai H, Yant SR, Storm TA, Fuess S, Meuse L, Kay MA. 2001. Extrachromosomal recombinant adeno-associated virus vector genomes are primarily responsible for stable liver transduction in vivo. J. Virol. 75:6969-76
65. Ni TH, Zhou X, McCarty DM, Zolotukhin I, Muzyczka N. 1994. In vitro replication of adeno-associated virus DNA. J. Virol. 68:1128-38
66. Oelze I, Rittner K, Sczakiel G. 1994. Adeno-associated virus type 2 rep gene-mediated inhibition of basal gene expression of human immunodeficiency virus type 1 involves its negative regulatory functions. J. Virol. 68:1229-33
67. Ogata T, Kozuka T, Kanda T. 2003. Identification of an insulator in AAVS1, a preferred region for integration of adeno-associated virus DNA. J. Virol. 77:9000-7
68. Pereira DJ, McCarty DM, Muzyczka N. 1997. The adeno-associated virus (AAV) Rep protein acts as both a repressor and an activator to regulate AAV transcription during a productive infection. J. Virol. 71:1079-88
69. Philpott NJ, Giraud-Wali C, Dupuis C, Gomos J, Hamilton H, et al. 2002. Efficient integration of recombinant adeno-associated virus DNA vectors requires a p5-rep sequence in cis. J. Virol. 76:5411-21
70. Philpott NJ, Gomos J, Berns KI, Falck-Pedersen E. 2002. A p5 integration efficiency element mediates Rep-dependent integration into AAVS1 at chromosome 19. Proc. Natl. Acad. Sci. USA 99:12381-85
71. Pieroni L, Fipaldini C, Monciotti A, Cimini D, Sgura A, et al. 1998. Targeted integration of adeno-associated virus-derived plasmids in transfected human cells. Virology 249:249-59
72. Ponnazhagan S, Erikson D, Kearns WG, Zhou SZ, Nahreini P, et al. 1997. Lack of site-specific integration of the recombinant adeno-associated virus 2 genomes in human cells. Hum. Gene Ther. 8:275-84
73. Porteus MH, Baltimore D. 2003. Chimeric nucleases stimulate gene targeting in human cells. Science 300:763
74. Porteus MH, Cathomen T, Weitzman MD, Baltimore D. 2003. Efficient gene targeting mediated by adeno-associated virus and DNA double-strand breaks. Mol. Cell Biol. 23:3558-65
75. Recchia A, Parks RJ, Lamartina S, Toniatti C, Pieroni L, et al. 1999. Site-specific integration mediated by a hybrid adenovirus/adeno-associated virus vector. Proc. Natl. Acad. Sci. USA 96:2615-20
76. Rinaudo D, Lamartina S, Roscilli G, Ciliberto G, Toniatti C. 2000. Conditional site-specific integration into human chromosome 19 by using a ligand-dependent chimeric adeno-associated virus/Rep protein. J. Virol 74:281-94
77. Rittner K, Heilbronn R, Kleinschmidt JA, Sczakiel G. 1992. Adeno-associated virus type 2-mediated inhibition of human immunodeficiency virus type 1 (HIV-1) replication: involvement of p78rep/p68rep and the HIV-1 long terminal repeat. J. Gen. Virol. 73:2977-81
78. Rizzuto G, Gorgoni B, Cappelletti M, Lazzaro D, Gloaguen I, et al. 1999. Development of animal models for adeno-associated virus site-specific integration. J. Virol. 73:2517-26
79. Russell DW. 2003. AAV loves an active genome. Nat. Genet. 34:241-42
80. Russell DW, Hirata RK. 1998. Human gene targeting by viral vectors. Nat. Genet. 18:325-30
81. Rutledge EA, Russell DW. 1997. Adeno-associated virus vector integration junctions. J. Virol. 71:8429-36
82. Ryan JH, Zolotukhin S, Muzyczka N. 1996. Sequence requirements for binding of Rep68 to the adeno-associated virus terminal repeats. J. Virol. 70:1542-53
83. Samulski RJ, Chang LS, Shenk T. 1989. Helper-free stocks of recombinant adeno-associated viruses: Normal integration does not require viral gene expression. J. Virol. 63:3822-28
84. Samulski RJ, Zhu X, Xiao X, Brook JD, Housman DE, et al. 1991. Targeted integration of adeno-associated virus (AAV) into human chromosome 19. EMBO J. 10:3941-50. Erratum. 1992. EMBO J. 11(3):1228
85. Samulski RJ, Zhu X, Xiao X, Brook JD, Housman DE, et al. 1991. Targeted integration of adeno-associated virus (AAV) into human chromosome 19. EMBO J. 10:3941-50. Erratum. 1992. EMBO J. 11(3):1228
86. Satoh W, Hirai Y, Tamayose K, Shimada T. 2000. Site-specific integration of an adeno-associated virus vector plasmid mediated by regulated expression of rep based on Cre-loxP recombination. J. Virol. 74:10631-38
87. Schnepp BC, Clark KR, Klemanski DL, Pacak CA, Johnson PR. 2003. Genetic fate of recombinant adeno-associated virus vector genomes in muscle. J. Virol. 77:3495-504
88. Schroder AR, Shinn P, Chen H, Berry C, Ecker JR, Bushman F. 2002. HIV-1 integration in the human genome favors active genes and local hotspots. Cell 110:521-29
89. Schulz M, Freisem-Rabien U, Jessberger R, Doerfler W. 1987. Transcriptional activities of mammalian genomes at sites of recombination with foreign DNA. J. Virol. 61:344-53
90. Snyder RO, Im D-S, Muzyczka N. 1990. Evidence for covalent attachment of the adeno-associated virus Rep protein to the ends of the AAV genome. J. Virol. 64:6204-13
91. Snyder RO, Im DS, Ni T, Xiao X, Samulski RJ, Muzyczka N. 1993. Features of the adeno-associated virus origin involved in substrate recognition by the viral Rep protein. J. Virol. 67:6096-104
92. Snyder RO, Samulski RJ, Muzyczka N. 1990. In vitro resolution of covalently joined AAV chromosome ends. Cell 60:105-33
93. Snyder RO, Spratt SK, Lagarde C, Bohl D, Kaspar B, et al. 1997. Efficient and stable adeno-associated virus-mediated transduction in the skeletal muscle of adult immunocompetent mice. Hum. Gene Ther. 8:1891-900
94. Sun L, Li J, Xiao X. 2000. Overcoming adeno-associated virus vector size limitation through viral DNA heterodimerization. Nat. Med. 6:599-602
95. Surosky RT, Urabe M, Godwin SG, McQuiston SA, Kurtzman GJ, et al. 1997. Adeno-associated virus Rep proteins target DNA sequences to a unique locus in the human genome. J. Virol. 71:7951-59
96. Tratschin JD, Miller IL, Smith MG, Carter BJ. 1985. Adeno-associated virus vector for high-frequency integration, expression, and rescue of genes in mammalian cells. Mol. Cell Biol. 5:3251-60
97. Urcelay E, Ward P, Wiener Sm, Safer B, Kotin Rm. 1995. Asymmetric replication in vitro from a human sequence element is dependent on adeno-associated virus Rep protein. J. Virol. 69:2038-46
98. Vincent-Lacaze N, Snyder RO, Gluzman R, Bohl D, Lagarde C, Danos O. 1999. Structure of adeno-associated virus vector DNA following transduction of the skeletal muscle. J. Virol. 73:1949-55
99. Wang Y, Camp SM, Niwano M, Shen X, Bakowska JC, et al. 2002. Herpes simplex virus type 1/adeno-associated virus rep(+) hybrid amplicon vector improves the stability of transgene expression in human cells by site-specific integration. J. Virol. 76:7150-62
100. Weitzman MD, Kyostio SR, Kotin RM, Owens RA. 1994. Adeno-associated virus (AAV) Rep proteins mediate complex formation between AAV DNA and its integration site in human DNA. Proc. Natl. Acad. Sci. USA 91:5808-12
101. Wonderling RS, Owens RA. 1997. Binding sites for adeno-associated virus Rep proteins within the human genome. J. Virol. 71:2528-34
102. Xiao X, Li J, Samulski RJ. 1996. Efficient long-term gene transfer into muscle tissue of immunocompetent mice by adeno-associated virus vector. J. Virol. 70:8098-108
103. Xiao X, Xiao W, Li J, Samulski RJ. 1997. A novel 165-base-pair terminal repeat sequence is the sole cis requirement for the adeno-associated virus life cycle. J. Virol. 71:941-48
104. Yalkinoglu AO, Heilbronn R, Burkle A, Schlehofer JR, zur-Hausen H. 1988. DNA amplification of adeno-associated virus as a response to cellular genotoxic stress. Cancer Res. 48:3123-32
105. Yalkinoglu AO, Zentgraf H, Hubscher U. 1991. Origin of adeno-associated virus DNA replication is a target of carcinogen-inducible DNA amplification. J. Virol. 65:3175-84
106. Yan Z, Zhang Y, Duan D, Engelhardt JF. 2000. Trans-splicing vectors expand the utility of adeno-associated virus for gene therapy. Proc. Natl. Acad. Sci. USA 97:6716-21
107. Yang CC, Xiao X, Zhu X, Ansardi DC, Epstein ND, et al. 1997. Cellular recombination pathways and viral terminal repeat hairpin structures are sufficient for adeno-associated virus integration in vivo and in vitro. J. Virol. 71:9231-47
108. Yang J, Zhou W, Zhang Y, Zidon T, Ritchie T, Engelhardt JF. 1999. Concatamerization of adeno-associated virus circular genomes occurs through intermolecular recombination. J. Virol. 73:9468-77
109. Young SM Jr, McCarty DM, Degtyareva N, Samulski RJ. 2000. Roles of adeno-associated virus Rep protein and human chromosome 19 in site-specific recombination. J. Virol. 74:3953-66
110. Young SM Jr, Samulski RJ. 2001. Adeno-associated virus (AAV) site-specific recombination does not require a Rep-dependent origin of replication within the AAV terminal repeat. Proc. Natl. Acad. Sci. USA 98:13525-30
111. Yue Y, Duan D. 2003. Double strand interaction is the predominant pathway for intermolecular recombination of adeno-associated viral genomes. Virology 313:1-7