Intracellular transport of recombinant adeno-associated virus vectors

Gene Therapy

Volumn 19, Issue 6, 2012, Pages 649-658

  Nonnenmacher, M ^a   Weber, T ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

adeno associated virus; intracellular trafficking; recombinant AAV biology

Indexed keywords

ADENOVIRUS VECTOR; PROTEASOME INHIBITOR; TYROSINE;

CELL ADHESION; CELL MIGRATION; ENDOCYTOSIS; GENE TARGETING; GENOME; HUMAN; INTRACELLULAR TRANSPORT; NONHUMAN; NUCLEAR IMPORT; PRIORITY JOURNAL; REVIEW; TARGET CELL; UBIQUITINATION; VIRUS CAPSID;

BIOLOGICAL TRANSPORT; DEPENDOVIRUS; ENDOCYTOSIS; GENE THERAPY; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; HUMANS; RECOMBINATION, GENETIC; TRANSDUCTION, GENETIC; TROPISM; VIRUS ATTACHMENT;

ADENO-ASSOCIATED VIRUS; ANIMALIA; MIRIDAE;

EID: 84861998784     PISSN: 09697128     EISSN: 14765462     Source Type: Journal    
DOI: 10.1038/gt.2012.6     Document Type: Review

References (164)

1. Kaneda Y. Update on non-viral delivery methods for cancer therapy: possibilities of a drug delivery system with anticancer activities beyond delivery as a new therapeutic tool. Expert Opin Drug Deliv 2010; 7: 1079-1093.
2. Cavazzana-Calvo M, Hacein-Bey S, de Saint Basile G, Gross F, Yvon E, Nusbaum P et al. Gene therapy of human severe combined immunodeficiency (SCID)-X1 disease. Science 2000; 288: 669-672. (Pubitemid 30241569)
3. Gaspar HB, Parsley KL, Howe S, King D, Gilmour KC, Sinclair J et al. Gene therapy of X-linked severe combined immunodeficiency by use of a pseudotyped gammaretroviral vector. Lancet 2004; 364: 2181-2187. (Pubitemid 40018447)
4. Kohn DB, Candotti F. Gene therapy fulfilling its promise. N Engl J Med 2009; 360: 518-521.
5. Simonelli F, Maguire AM, Testa F, Pierce EA, Mingozzi F, Bennicelli JL et al. Gene therapy for Leber's congenital amaurosis is safe and effective through 1.5 years after vector administration. Mol Ther 2010; 18: 643-650.
6. Maguire AM, High KA, Auricchio A, Wright JF, Pierce EA, Testa F et al. Age-dependent effects of RPE65 gene therapy for Leber's congenital amaurosis: a phase 1 dose-escalation trial. Lancet 2009; 374: 1597-1605.
7. Herzog RW, Cao O, Srivastava A. Two decades of clinical gene therapy-success is finally mounting. Discov Med 2010; 9: 105-111.
8. Hoggan MD, Blacklow NR, Rowe WP. Studies of small DNA viruses found in various adenovirus preparations: physical, biological, and immunological characteristics. Proc Natl Acad Sci USA 1966; 55: 1467-1474.
9. KerrJR.Parvoviruses. Hodder Arnold; Distributed in the United States of America by Oxford University Press: London, New York, 2006.
10. Sun JY, Anand-Jawa V, Chatterjee S, Wong KK. Immune responses to adenoassociated virus and its recombinant vectors. Gene Therapy 2003; 10: 964-976. (Pubitemid 36722431)
11. Sonntag F, Schmidt K, Kleinschmidt JA. A viral assembly factor promotes AAV2 capsid formation in the nucleolus. Proc Natl Acad Sci USA 2010; 107: 10220-10225.
12. 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 USA 1982; 79: 2077-2081. (Pubitemid 12120800)
13. Laughlin CA, Tratschin JD, Coon H, Carter BJ. Cloning of infectious adeno-associated virus genomes in bacterial plasmids. Gene 1983; 23: 65-73.
14. Hermonat PL, Muzyczka N. 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 1984; 81: 6466-6470. (Pubitemid 15221855)
15. Tratschin JD, West MH, Sandbank T, Carter BJ. A human parvovirus, adeno-associated virus, as a eucaryotic vector: transient expression and encapsidation of the procaryotic gene for chloramphenicol acetyltransferase. Mol Cell Biol 1984; 4: 2072-2081. (Pubitemid 15209979)
16. Dong JY, Fan PD, Frizzell RA. Quantitative analysis of the packaging capacity of recombinant adeno-associated virus. Hum Gene Ther 1996; 7: 2101-2112. (Pubitemid 26400735)
17. Duan D, Yan Z, Yue Y, Ding W, Engelhardt JF. Enhancement of muscle gene delivery with pseudotyped adeno-associated virus type 5 correlates with myoblast differentiation. J Virol 2001; 75: 7662-7671. (Pubitemid 32738024)
18. Rabinowitz JE, Rolling F, Li C, Conrath H, Xiao W, Xiao X et al. Cross-packaging of a single adeno-associated virus (AAV) type 2 vector genome into multiple AAV serotypes enables transduction with broad specificity. J Virol 2002; 76: 791-801. (Pubitemid 34033377)
19. Grimm D, Kay MA. From virus evolution to vector revolution: use of naturally occurring serotypes of adeno-associated virus (AAV) as novel vectors for human gene therapy. Curr Gene Ther 2003; 3: 281-304.
20. 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 2008; 16: 1073-1080. (Pubitemid 351737072)
21. Wu Z, Asokan A, Samulski RJ. Adeno-associated virus serotypes: vector toolkit for human gene therapy. Mol Ther 2006; 14: 316-327. (Pubitemid 44184972)
22. Podsakoff G, Wong Jr. KK, Chatterjee S. Efficient gene transfer into nondividing cells by adeno-associated virus-based vectors. J Virol 1994; 68: 5656-5666.
23. Gao GP, Alvira MR, Wang L, Calcedo R, Johnston J, Wilson JM. Novel adenoassociated viruses from rhesus monkeys as vectors for human gene therapy. Proc Natl Acad Sci USA 2002; 99: 11854-11859. (Pubitemid 34994488)
24. Zincarelli C, Soltys S, Rengo G, Koch WJ, Rabinowitz JE. Comparative cardiac gene delivery of adeno-associated virus serotypes 1-9 reveals that AAV6 mediates the most efficient transduction in mouse heart. Clin Transl Sci 2010; 3: 81-89.
25. Summerford C, Samulski RJ. Membrane-associated heparan sulfate proteoglycan is a receptor for adeno-associated virus type 2 virions. J Virol 1998; 72: 1438-1445. (Pubitemid 28116931)
26. Qing K, Mah C, Hansen J, Zhou S, Dwarki V, Srivastava A. Human fibroblast growth factor receptor 1 is a co-receptor for infection by adeno-associated virus 2. Nat Med 1999; 5: 71-77. (Pubitemid 29051001)
27. Summerford C, Bartlett JS, Samulski RJ. AlphaVbeta5 integrin: a co-receptor for adeno-associated virus type 2 infection. Nat Med 1999; 5: 78-82. (Pubitemid 29051002)
28. Asokan A, Hamra JB, Govindasamy L, Agbandje-McKenna M, Samulski RJ. Adenoassociated virus type 2 contains an integrin alpha5beta1 binding domain essential for viral cell entry. J Virol 2006; 80: 8961-8969. (Pubitemid 44359970)
29. Akache B, Grimm D, Pandey K, Yant SR, Xu H, Kay MA. The 37/67-kilodalton laminin receptor is a receptor for adeno-associated virus serotypes 8, 2, 3, and 9. J Virol 2006; 80: 9831-9836. (Pubitemid 44435657)
30. Kashiwakura Y, Tamayose K, Iwabuchi K, Hirai Y, Shimada T, Matsumoto K et al. Hepatocyte growth factor receptor is a coreceptor for adeno-associated virus type 2 infection. J Virol 2005; 79: 609-614. (Pubitemid 39648414)
31. Qiu J, Brown KE. Integrin alphaVbeta5 is not involved in adeno-associated virus type 2 (AAV2) infection. Virology 1999; 264: 436-440.
32. Wallen AJ, Barker GA, Fein DE, Jing H, Diamond SL. Enhancers of adeno-associated virus AAV2 transduction via high throughput siRNA screening. Mol Ther 2011; 19: 1152-1160.
33. Chen CL, Jensen RL, Schnepp BC, Connell MJ, Shell R, Sferra TJ et al. Molecular characterization of adeno-associated viruses infecting children. J Virol 2005; 79: 14781-14792. (Pubitemid 41636276)
34. Kern A, Schmidt K, Leder C, Muller OJ, Wobus CE, Bettinger K et al. Identification of a heparin-binding motif on adeno-associated virus type 2 capsids. J Virol 2003; 77: 11072-11081. (Pubitemid 37204297)
35. Kalia M, Jameel S. Virus entry paradigms. Amino Acids 2011; 41: 1147-1157.
36. Kan M, Wang F, Xu J, Crabb JW, Hou J, McKeehan WL. An essential heparinbinding domain in the fibroblast growth factor receptor kinase. Science 1993; 259: 1918-1921. (Pubitemid 23124467)
37. Schmidt M, Chiorini JA. Gangliosides are essential for bovine adeno-associated virus entry. J Virol 2006; 80: 5516-5522.
38. Levy HC, Bowman VD, Govindasamy L, McKenna R, Nash K, Warrington K et al. Heparin binding induces conformational changes in adeno-associated virus serotype 2. J Struct Biol 2009; 165: 146-156.
39. Duan D, Li Q, Kao AW, Yue Y, Pessin JE, Engelhardt JF. Dynamin is required for recombinant adeno-associated virus type 2 infection. J Virol 1999; 73: 10371-10376.
40. Bartlett JS, Wilcher R, Samulski RJ. Infectious entry pathway of adeno-associated virus and adeno-associated virus vectors. J Virol 2000; 74: 2777-2785. (Pubitemid 30117589)
41. Mayor S, Pagano RE. Pathways of clathrin-independent endocytosis. Nat Rev Mol Cell Biol 2007; 8: 603-612. (Pubitemid 47106613)
42. Doherty GJ, McMahon HT. Mechanisms of endocytosis. Annu Rev Biochem 2009; 78: 857-902.
43. Sanlioglu S, Benson PK, Yang J, Atkinson EM, Reynolds T, Engelhardt JF. Endocytosis and nuclear trafficking of adeno-associated virus type 2 are controlled by rac1 and phosphatidylinositol-3 kinase activation. J Virol 2000; 74: 9184-9196.
44. Sanlioglu AD, Karacay B, Benson PK, Engelhardt JF, Sanlioglu S. Novel approaches to augment adeno-associated virus type-2 endocytosis and transduction. Virus Res 2004; 104: 51-59. (Pubitemid 38721263)
45. Ridley AJ, Paterson HF, Johnston CL, Diekmann D, Hall A. The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell 1992; 70: 401-410.
46. Lamaze C, Chuang TH, Terlecky LJ, Bokoch GM, Schmid SL. Regulation of receptormediated endocytosis by Rho and Rac. Nature 1996; 382: 177-179. (Pubitemid 26242886)
47. Malecz N, McCabe PC, Spaargaren C, Qiu R, Chuang Y, Symons M. Synaptojanin 2, a novel Rac1 effector that regulates clathrin-mediated endocytosis. Curr Biol 2000; 10: 1383-1386.
48. Meier O, Greber UF. Adenovirus endocytosis. J Gene Med 2004; 6(Suppl 1): S152-S163. (Pubitemid 40228024)
49. Nonnenmacher M, Weber T. Adeno-associated virus 2 infection requires endocytosis through the CLIC/GEEC pathway. Cell Host Microbe 2011; 10: 563-576.
50. Wittrup A, Zhang SH, Svensson KJ, Kucharzewska P, Johansson MC, Morgelin M et al. Magnetic nanoparticle-based isolation of endocytic vesicles reveals a role of the heat shock protein GRP75 in macromolecular delivery. Proc Natl Acad Sci USA 2010; 107: 13342-13347.
51. Douar AM, Poulard K, Stockholm D, Danos O. Intracellular trafficking of adenoassociated virus vectors: routing to the late endosomal compartment and proteasome degradation. J Virol 2001; 75: 1824-1833. (Pubitemid 32110172)
52. Richardson WD, Westphal H. A cascade of adenovirus early functions is required for expression of adeno-associated virus. Cell 1981; 27 (1 Part 2): 133-141. (Pubitemid 12205978)
53. Johnson J, Li C, Diprimio N, Weinberg M, McCown T, Samulski R. Mutagenesis of adeno-associated virus type 2 capsid protein VP1 uncovers new roles for basic amino acids in trafficking and cell-specific transduction. J Virol 2010; 84: 8888-8902.
54. Xiao W, Warrington Jr. KH, Hearing P, Hughes J, Muzyczka N. Adenovirus-facilitated nuclear translocation of adeno-associated virus type 2. J Virol 2002; 76: 11505-11517. (Pubitemid 35231307)
55. Rafii S, Dias S, Meeus S, Hattori K, Ramachandran R, Feuerback F et al. Infection of endothelium with E1(-)E4(+), but not E1(-)E4(-), adenovirus gene transfer vectors enhances leukocyte adhesion and migration by modulation of ICAM-1, VCAM-1, CD34, and chemokine expression. Circ Res 2001; 88: 903-910. (Pubitemid 32441468)
56. Chung SH, Frese KK, Weiss RS, Prasad BV, Javier RT. A new crucial protein interaction element that targets the adenovirus E4-ORF1 oncoprotein to membrane vesicles. J Virol 2007; 81: 4787-4797. (Pubitemid 46668675)
57. Thomas MA, Broughton RS, Goodrum FD, Ornelles DA. E4orf1 limits the oncolytic potential of the E1B-55K deletion mutant adenovirus. J Virol 2009; 83: 2406-2416.
58. Bantel-Schaal U, Braspenning-Wesch I, Kartenbeck J. Adeno-associated virus type 5 exploits two different entry pathways in human embryo fibroblasts. J Gen Virol 2009; 90. (Part 2): 317-322.
59. Bantel-Schaal U, Hub B, Kartenbeck J. Endocytosis of adeno-associated virus type 5 leads to accumulation of virus particles in the Golgi compartment. J Virol 2002; 76: 2340-2349. (Pubitemid 34150702)
60. Keiser NW, Yan Z, Zhang Y, Lei-Butters DC, Engelhardt JF. Unique characteristics of AAV1, 2, and 5 viral entry, intracellular trafficking, and nuclear import define transduction efficiency in HeLa cells. Hum Gene Ther 2011; 22: 1433-1444.
61. Hansen J, Qing K, Kwon HJ, Mah C, Srivastava A. Impaired intracellular trafficking of adeno-associated virus type 2 vectors limits efficient transduction of murine fibroblasts. J Virol 2000; 74: 992-996. (Pubitemid 30036236)
62. Miao CH, Nakai H, Thompson AR, Storm TA, Chiu W, Snyder RO et al. Nonrandom transduction of recombinant adeno-associated virus vectors in mouse hepatocytes in vivo: cell cycling does not influence hepatocyte transduction. J Virol 2000; 74: 3793-3803. (Pubitemid 30180322)
63. Di Pasquale G, Chiorini J. AAV transcytosis through barrier epithelia and endothelium. Mol Ther 2006; 13: 506-516. (Pubitemid 43257618)
64. Di Pasquale G, Kaludov N, Agbandje-McKenna M, Chiorini JA. BAAV transcytosis requires an interaction with beta-1-4 linked-glucosamine and gp96. PLoS ONE 2010; 5: e9336.
65. Sonntag F, Bleker S, Leuchs B, Fischer R, Kleinschmidt JA. Adeno-associated virus type 2 capsids with externalized VP1/VP2 trafficking domains are generated prior to passage through the cytoplasm and are maintained until uncoating occurs in the nucleus. J Virol 2006; 80: 11040-11054. (Pubitemid 44706545)
66. Pajusola K, Gruchala M, Joch H, Luscher TF, Yla-Herttuala S, Bueler H. Cell-typespecific characteristics modulate the transduction efficiency of adeno-associated virus type 2 and restrain infection of endothelial cells. J Virol 2002; 76: 11530-11540. (Pubitemid 35231309)
67. Ding W, Zhang LN, Yeaman C, Engelhardt JF. rAAV2 traffics through both the late and the recycling endosomes in a dose-dependent fashion. Mol Ther 2006; 13: 671-682.
68. Bonifacino JS, Rojas R. Retrograde transport from endosomes to the trans-Golgi network. Nat Rev Mol Cell Biol 2006; 7: 568-579. (Pubitemid 44325348)
69. Johannes L, Popoff V. Tracing the retrograde route in protein trafficking. Cell 2008; 135: 1175-1187.
70. Pelkmans L, Kartenbeck J, Helenius A. Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nat Cell Biol 2001; 3: 473-483. (Pubitemid 32422083)
71. Mannova P, Forstova J. Mouse polyomavirus utilizes recycling endosomes for a traffic pathway independent of COPI vesicle transport. J Virol 2003; 77: 1672-1681. (Pubitemid 36109979)
72. Spooner RA, Smith DC, Easton AJ, Roberts LM, Lord JM. Retrograde transport pathways utilised by viruses and protein toxins. J Virol 2006; 3: 26.
73. Nam HJ, Gurda BL, McKenna R, Potter M, Byrne B, Salganik M et al. Structural studies of adeno-associated virus serotype 8 capsid transitions associated with endosomal trafficking. J Virol 2011; 85: 11791-11799.
74. Kronenberg S, Bottcher B, von der Lieth CW, Bleker S, Kleinschmidt JA. A conformational change in the adeno-associated virus type 2 capsid leads to the exposure of hidden VP1 N termini. J Virol 2005; 79: 5296-5303. (Pubitemid 40548198)
75. Girod A, Wobus CE, Zadori Z, Ried M, Leike K, Tijssen P et al. The VP1 capsid protein of adeno-associated virus type 2 is carrying a phospholipase A2 domain required for virus infectivity. J Gen Virol 2002; 83 (Part 5): 973-978. (Pubitemid 34477268)
76. Grieger JC, Johnson JS, Gurda-Whitaker B, Agbandje-McKenna M, Samulski RJ. Surface-exposed adeno-associated virus Vp1-NLS capsid fusion protein rescues infectivity of noninfectious wild-type Vp2/Vp3 and Vp3-only capsids but not that of fivefold pore mutant virions. J Virol 2007; 81: 7833-7843. (Pubitemid 47101469)
77. Stahnke S, Lux K, Uhrig S, Kreppel F, Hösel M, Coutelle O et al. Intrinsic phospholipase A2 activity of adeno-associated virus is involved in endosomal escape of incoming particles. Virology 2011; 409: 77-83.
78. Stahnke S, Lux K, Uhrig S, Kreppel F, Hosel M, Coutelle O et al. Intrinsic phospholipase A2 activity of adeno-associated virus is involved in endosomal escape of incoming particles. Virology 2011; 409: 77-83.
79. Grieger JC, Snowdy S, Samulski RJ. Separate basic region motifs within the adeno-associated virus capsid proteins are essential for infectivity and assembly. J Virol 2006; 80: 5199-5210.
80. Richards RM, Lowy DR, Schiller JT, Day PM. Cleavage of the papillomavirus minor capsid protein, L2, at a furin consensus site is necessary for infection. Proc Natl Acad Sci USA 2006; 103: 1522-1527. (Pubitemid 43191198)
81. Magnuson B, Rainey EK, Benjamin T, Baryshev M, Mkrtchian S, Tsai B. ERp29 triggers a conformational change in polyomavirus to stimulate membrane binding. Mol Cell 2005; 20: 289-300. (Pubitemid 41484173)
82. Wang K, Guan T, Cheresh DA, Nemerow GR. Regulation of adenovirus membrane penetration by the cytoplasmic tail of integrin beta5. J Virol 2000; 74: 2731-2739. (Pubitemid 30117584)
83. Johnson JS, Gentzsch M, Zhang L, Ribeiro CM, Kantor B, Kafri T et al. AAV exploits subcellular stress associated with inflammation, endoplasmic reticulum expansion, and misfolded proteins in models of cystic fibrosis. PLoS Pathog 2011; 7: e1002053.
84. Akache B, Grimm D, Shen X, Fuess S, Yant SR, Glazer DS et al. A two-hybrid screen identifies cathepsins B and L as uncoating factors for adeno-associated virus 2 and 8. Mol Ther 2007; 15: 330-339. (Pubitemid 46111883)
85. Thomas CE, Storm TA, Huang Z, Kay MA. Rapid uncoating of vector genomes is the key to efficient liver transduction with pseudotyped adeno-associated virus vectors. J Virol 2004; 78: 3110-3122. (Pubitemid 38314369)
86. Johnson J, Samulski R. Enhancement of adeno-associated virus infection by mobilizing capsids into and out of the nucleolus. J Virol 2009; 83: 2632-2644.
87. Hoque M, Ishizu K, Matsumoto A, Han SI, Arisaka F, Takayama M et al. Nuclear transport of the major capsid protein is essential for adeno-associated virus capsid formation. J Virol 1999; 73: 7912-7915. (Pubitemid 29383285)
88. Gorlich D, Kostka S, Kraft R, Dingwall C, Laskey RA, Hartmann E et al. Two different subunits of importin cooperate to recognize nuclear localization signals and bind them to the nuclear envelope. Curr Biol 1995; 5: 383-392.
89. Gorlich D, Kutay U. Transport between the cell nucleus and the cytoplasm. Annu Rev Cell Dev Biol 1999; 15: 607-660. (Pubitemid 32250388)
90. Lee BJ, Cansizoglu AE, Suel KE, Louis TH, Zhang Z, Chook YM. Rules for nuclear localization sequence recognition by karyopherin beta 2. Cell 2006; 126: 543-558. (Pubitemid 44163605)
91. Qiu J, Brown KE. A 110-kDa nuclear shuttle protein, nucleolin, specifically binds to adeno-associated virus type 2 (AAV-2) capsid. Virology 1999; 257: 373-382. (Pubitemid 29393405)
92. Bevington JM, Needham PG, Verrill KC, Collaco RF, Basrur V, Trempe JP. Adeno-associated virus interactions with B23/Nucleophosmin: identification of sub-nucleolar virion regions. Virology 2007; 357: 102-113. (Pubitemid 44820332)
93. Cotmore SF, D'Abramo Jr. AM, Ticknor CM, Tattersall P. Controlled conformational transitions in the MVM virion expose the VP1 N-terminus and viral genome without particle disassembly. Virology 1999; 254: 169-181. (Pubitemid 29391724)
94. Ros C, Baltzer C, Mani B, Kempf C. Parvovirus uncoating in vitro reveals a mechanism of DNA release without capsid disassembly and striking differences in encapsidated DNA stability. Virology 2006; 345: 137-147. (Pubitemid 43107579)
95. Sipo I, Fechner H, Pinkert S, Suckau L, Wang X, Weger S et al. Differential internalization and nuclear uncoating of self-complementary adeno-associated virus pseudotype vectors as determinants of cardiac cell transduction. Gene Therapy 2007; 14: 1319-1329. (Pubitemid 47370845)
96. Duan D, Yue Y, Yan Z, Yang J, Engelhardt JF. Endosomal processing limits gene transfer to polarized airway epithelia by adeno-associated virus. J Clin Invest 2000; 105: 1573-1587. (Pubitemid 30390308)
97. Yan Z, Zak R, Luxton GW, Ritchie TC, Bantel-Schaal U, Engelhardt JF. Ubiquitination of both adeno-associated virus type 2 and 5 capsid proteins affects the transduction efficiency of recombinant vectors. J Virol 2002; 76: 2043-2053. (Pubitemid 34150672)
98. Zhong L, Zhao W, Wu J, Li B, Zolotukhin S, Govindasamy L et al. A dual role of EGFR protein tyrosine kinase signaling in ubiquitination of AAV2 capsids and viral secondstrand DNA synthesis. Mol Ther 2007; 15: 1323-1330. (Pubitemid 46965329)
99. Zhong L, Qing K, Si Y, Chen L, Tan M, Srivastava A. Heat-shock treatment-mediated increase in transduction by recombinant adeno-associated virus 2 vectors is independent of the cellular heat-shock protein 90. J Biol Chem 2004; 279: 12714-12723. (Pubitemid 38445843)
100. Sanlioglu S, Engelhardt JF. Cellular redox state alters recombinant adeno-associated virus transduction through tyrosine phosphatase pathways. Gene Therapy 1999; 6: 1427-1437. (Pubitemid 29396731)
101. Latonen L, Moore HM, Bai B, Jaamaa S, Laiho M. Proteasome inhibitors induce nucleolar aggregation of proteasome target proteins and polyadenylated RNA by altering ubiquitin availability. Oncogene 2011; 30: 790-805.
102. Condemine W, Takahashi Y, Le Bras M, de The H. A nucleolar targeting signal in PML-I addresses PML to nucleolar caps in stressed or senescent cells. J Cell Sci 2007; 120 (Part 18): 3219-3227. (Pubitemid 350018413)
103. Mattsson K, Pokrovskaja K, Kiss C, Klein G, Szekely L. Proteins associated with the promyelocytic leukemia gene product (PML)-containing nuclear body move to the nucleolus upon inhibition of proteasome-dependent protein degradation. Proc Natl Acad Sci USA 2001; 98: 1012-1017. (Pubitemid 32121178)
104. Opie SR, Warrington Jr. KH, Agbandje-McKenna M, Zolotukhin S, Muzyczka N. Identification of amino acid residues in the capsid proteins of adeno-associated virus type 2 that contribute to heparan sulfate proteoglycan binding. J Virol 2003; 77: 6995-7006. (Pubitemid 36666892)
105. Wu P, Xiao W, Conlon T, Hughes J, Agbandje-McKenna M, Ferkol T et al. Mutational analysis of the adeno-associated virus type 2 (AAV2) capsid gene and construction of AAV2 vectors with altered tropism. J Virol 2000; 74: 8635-8647. (Pubitemid 30666714)
106. Qing K, Khuntirat B, Mah C, Kube DM, Wang XS, Ponnazhagan S et al. 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 1998; 72: 1593-1599. (Pubitemid 28116947)
107. Qing K, Wang XS, Kube DM, Ponnazhagan S, Bajpai A, Srivastava A. Role of tyrosine phosphorylation of a cellular protein in adeno-associated virus 2-mediated transgene expression. Proc Natl Acad Sci USA 1997; 94: 10879-10884.
108. Mah C, Qing K, Khuntirat B, Ponnazhagan S, Wang XS, Kube DM et al. Adeno-associated virus type 2-mediated gene transfer: role of epidermal growth factor receptor protein tyrosine kinase in transgene expression. J Virol 1998; 72: 9835-9843. (Pubitemid 28520849)
109. Fisher KJ, Gao GP, Weitzman MD, DeMatteo R, Burda JF, Wilson JM. Transduction with recombinant adeno-associated virus for gene therapy is limited by leading-strand synthesis. J Virol 1996; 70: 520-532. (Pubitemid 126508820)
110. Jayandharan GR, Zhong L, Li B, Kachniarz B, Srivastava A. Strategies for improving the transduction efficiency of single-stranded adeno-associated virus vectors in vitro and in vivo. Gene Therapy 2008; 15: 1287-1293.
111. Zhong L, Li B, Jayandharan G, Mah C, Govindasamy L, Agbandje-McKenna M et al. Tyrosine-phosphorylation of AAV2 vectors and its consequences on viral intracellular trafficking and transgene expression. Virology 2008; 381: 194-202.
112. Li M, Jayandharan G, Li B, Ling C, Ma W, Srivastava A et al. High-efficiency transduction of fibroblasts and mesenchymal stem cells by tyrosine-mutant AAV2 vectors for their potential use in cellular therapy. Hum Gene Ther 2010; 21: 1527-1543.
113. Jayandharan GR, Zhong L, Sack BK, Rivers AE, Li M, Li B et al. Optimized adenoassociated virus (AAV)-protein phosphatase-5 helper viruses for efficient liver transduction by single-stranded AAV vectors: therapeutic expression of factor IX at reduced vector doses. Hum Gene Ther 2010; 21: 271-283.
114. Markusic DM, Herzog RW, Aslanidi GV, Hoffman BE, Li B, Li M et al. High-efficiency transduction and correction of murine hemophilia B using AAV2 vectors devoid of multiple surface-exposed tyrosines. Mol Ther 2010; 18: 2048-2056.
115. Petrs-Silva H, Dinculescu A, Li Q, Deng W-T, Pang J-J, Min S-H et al. Novel properties of tyrosine-mutant AAV2 vectors in the mouse retina. Mol Ther 2011; 19: 293-301.
116. Petrs-Silva H, Dinculescu A, Li Q, Min S-H, Chiodo V, Pang J-J et al. High-efficiency transduction of the mouse retina by tyrosine-mutant AAV serotype vectors. Mol Ther 2009; 17: 463-471.
117. Qiao C, Zhang W, Yuan Z, Shin JH, Li J, Jayandharan GR et al. Adeno-associated virus serotype 6 capsid tyrosine-to-phenylalanine mutations improve gene transfer to skeletal muscle. Hum Gene Ther 2010; 21: 1343-1348.
118. Grimm D, Kern A, Pawlita M, Ferrari F, Samulski R, Kleinschmidt J. Titration of AAV-2 particles via a novel capsid ELISA: packaging of genomes can limit production of recombinant AAV-2. Gene Therapy 1999; 6: 1322-1330. (Pubitemid 29359028)
119. Zeltner N, Kohlbrenner E, Clement N, Weber T, Linden RM. Near-perfect infectivity of wild-type AAV as benchmark for infectivity of recombinant AAV vectors. Gene Therapy 2010; 17: 872-879.
120. Chapman MS, Rossmann MG. Single-stranded DNA-protein interactions in canine parvovirus. Structure 1995; 3: 151-162.
121. Lang SI, Boelz S, Stroh-Dege AY, Rommelaere J, Dinsart C, Cornelis JJ. The infectivity and lytic activity of minute virus of mice wild-type and derived vector particles are strikingly different. J Virol 2005; 79: 289-298. (Pubitemid 39648384)
122. Ng R, Govindasamy L, Gurda BL, McKenna R, Kozyreva OG, Samulski RJ et al. Structural characterization of the dual glycan binding adeno-associated virus serotype 6. J Virol 2010; 84: 12945-12957.
123. Wu Z, Miller E, Agbandje-McKenna M, Samulski RJ. Alpha2,3 and alpha2,6 N-linked sialic acids facilitate efficient binding and transduction by adeno-associated virus types 1 and 6. J Virol 2006; 80: 9093-9103. (Pubitemid 44359983)
124. Chao H, Liu Y, Rabinowitz J, Li C, Samulski RJ, Walsh CE. Several log increase in therapeutic transgene delivery by distinct adeno-associated viral serotype vectors. Mol Ther 2000; 2: 619-623.
125. Wang C, Wang CM, Clark KR, Sferra TJ. Recombinant AAV serotype 1 transduction efficiency and tropism in the murine brain. Gene Therapy 2003; 10: 1528-1534. (Pubitemid 36987147)
126. 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. (Pubitemid 351517093)
127. Loiler SA, Tang Q, Clarke T, Campbell-Thompson ML, Chiodo V, Hauswirth W et al. Localized gene expression following administration of adeno-associated viral vectors via pancreatic ducts. Mol Ther 2005; 12: 519-527. (Pubitemid 41150138)
128. Kurzeder C, Koppold B, Sauer G, Pabst S, Kreienberg R, Deissler H. CD9 promotes adeno-associated virus type 2 infection of mammary carcinoma cells with low cell surface expression of heparan sulphate proteoglycans. Int J Mol Med 2007; 19: 325-333.
129. Richter M, Iwata A, Nyhuis J, Nitta Y, Miller AD, Halbert CL et al. Adeno-associated virus vector transduction of vascular smooth muscle cells in vivo. Physiol Genomics 2000; 2: 117-127.
130. Manno CS, Chew AJ, Hutchison S, Larson PJ, Herzog RW, Arruda VR et al. AAVmediated factor IX gene transfer to skeletal muscle in patients with severe hemophilia B. Blood 2003; 101: 2963-2972. (Pubitemid 36857981)
131. Bartlett JS, Samulski RJ, McCown TJ. Selective and rapid uptake of adeno-associated virus type 2 in brain. Hum Gene Ther 1998; 9: 1181-1186. (Pubitemid 28269004)
132. Koeberl DD, Alexander IE, Halbert CL, Russell DW, Miller AD. Persistent expression of human clotting factor IX from mouse liver after intravenous injection of adeno-associated virus vectors. Proc Natl Acad Sci USA 1997; 94: 1426-1431. (Pubitemid 27087867)
133. Takeda S, Takahashi M, Mizukami H, Kobayashi E, Takeuchi K, Hakamata Y et al. Successful gene transfer using adeno-associated virus vectors into the kidney: comparison among adeno-associated virus serotype 1-5 vectors in vitro and in vivo. Nephron Exp Nephrol 2004; 96: e119-e126.
134. Blackburn SD, Steadman RA, Johnson FB. Attachment of adeno-associated virus type 3H to fibroblast growth factor receptor 1. Arch Virol 2006; 151: 617-623.
135. Ling C, Lu Y, Kalsi JK, Jayandharan GR, Li B, Ma W et al. Human hepatocyte growth factor receptor is a cellular coreceptor for adeno-associated virus serotype 3. Hum Gene Ther 2010; 21: 1741-1747.
136. Glushakova LG, Lisankie MJ, Eruslanov EB, Ojano-Dirain C, Zolotukhin I, Liu C et al. AAV3-mediated transfer and expression of the pyruvate dehydrogenase E1 alpha subunit gene causes metabolic remodeling and apoptosis of human liver cancer cells. Mol Genet Metab 2009; 98: 289-299.
137. Kaludov N, Brown KE, Walters RW, Zabner J, Chiorini JA. Adeno-associated virus serotype 4 (AAV4) and AAV5 both require sialic acid binding for hemagglutination and efficient transduction but differ in sialic acid linkage specificity. J Virol 2001; 75: 6884-6893. (Pubitemid 32641575)
138. Davidson BL, Stein CS, Heth JA, Martins I, Kotin RM, Derksen TA et al. Recombinant adeno-associated virus type 2, 4, and 5 vectors: transduction of variant cell types and regions in the mammalian central nervous system. Proc Natl Acad Sci USA 2000; 97: 3428-3432. (Pubitemid 30183319)
139. Weber M, Rabinowitz J, Provost N, Conrath H, Folliot S, Briot D et al. Recombinant adeno-associated virus serotype 4 mediates unique and exclusive long-term transduction of retinal pigmented epithelium in rat, dog, and nonhuman primate after subretinal delivery. Mol Ther 2003; 7: 774-781. (Pubitemid 36790254)
140. Walters RW, Yi SM, Keshavjee S, Brown KE, Welsh MJ, Chiorini JA et al. Binding of adeno-associated virus type 5 to 2,3-linked sialic acid is required for gene transfer. J Biol Chem 2001; 276: 20610-20616.
141. Di Pasquale G, Davidson BL, Stein CS, Martins I, Scudiero D, Monks A et al. Identification of PDGFR as a receptor for AAV-5 transduction. Nat Med 2003; 9: 1306-1312. (Pubitemid 37279855)
142. Seiler MP, Miller AD, Zabner J, Halbert CL. Adeno-associated virus types 5 and 6 use distinct receptors for cell entry. Hum Gene Ther 2006; 17: 10-19. (Pubitemid 43100511)
143. Weller ML, Amornphimoltham P, Schmidt M, Wilson PA, Gutkind JS, Chiorini JA. Epidermal growth factor receptor is a co-receptor for adeno-associated virus serotype 6. Nat Med 2010; 16: 662-664.
144. Blankinship MJ, Gregorevic P, Allen JM, Harper SQ, Harper H, Halbert CL et al. Efficient transduction of skeletal muscle using vectors based on adeno-associated virus serotype 6. Mol Ther 2004; 10: 671-678. (Pubitemid 39272856)
145. Gregorevic P, Blankinship MJ, Allen JM, Crawford RW, Meuse L, Miller DG et al. Systemic delivery of genes to striated muscles using adeno-associated viral vectors. Nat Med 2004; 10: 828-834. (Pubitemid 39070856)
146. Halbert CL, Allen JM, Miller AD. Adeno-associated virus type 6 (AAV6) vectors mediate efficient transduction of airway epithelial cells in mouse lungs
147. Allocca M, Mussolino C, Garcia-Hoyos M, Sanges D, Iodice C, Petrillo M et al. Novel adeno-associated virus serotypes efficiently transduce murine photoreceptors. J Virol 2007; 81: 11372-11380. (Pubitemid 47536108)
148. Taymans JM, Vandenberghe LH, Haute CV, Thiry I, Deroose CM, Mortelmans L et al. Comparative analysis of adeno-associated viral vector serotypes 1, 2, 5, 7, and 8 in mouse brain. Hum Gene Ther 2007; 18: 195-206. (Pubitemid 46626459)
149. Wang Z, Zhu T, Qiao C, Zhou L, Wang B, Zhang J et al. Adeno-associated virus serotype 8. efficiently delivers genes to muscle and heart. Nat Biotechnol 2005; 23: 321-328. (Pubitemid 41094420)
150. Nakai H, Fuess S, Storm TA, Muramatsu S, Nara Y, Kay MA. Unrestricted hepatocyte transduction with adeno-associated virus serotype 8 vectors in mice. J Virol 2005; 79: 214-224. (Pubitemid 39650967)
151. Shen S, Byrant KD, Brown SM, Randell SH, Asokan A. Terminal N-linked galactose is the primary receptor for adeno-associated virus 9. J Biol Chem 2011.
152. Vandendriessche T, Thorrez L, Acosta-Sanchez A, Petrus I, Wang L, Ma L et al. Efficacy and safety of adeno-associated viral vectors based on serotype 8 and 9 vs. lentiviral vectors for hemophilia B gene therapy. J Thromb Haemost 2007; 5: 16-24. (Pubitemid 44921062)
153. Inagaki K, Fuess S, Storm TA, Gibson GA, McTiernan CF, Kay MA et al. Robust systemic transduction with AAV9 vectors in mice: efficient global cardiac gene transfer superior to that of AAV8. Mol Ther 2006; 14: 45-53. (Pubitemid 43899488)
154. Foust KD, Nurre E, Montgomery CL, Hernandez A, Chan CM, Kaspar BK. Intravascular AAV9 preferentially targets neonatal neurons and adult astrocytes. Nat Biotechnol 2009; 27: 59-65.
155. Yue Y, Shin JH, Duan D. Whole body skeletal muscle transduction in neonatal dogs with AAV-9. Methods Mol Biol 2011; 709: 313-329.
156. Bostick B, Ghosh A, Yue Y, Long C, Duan D. Systemic AAV-9 transduction in mice is influenced by animal age but not by the route of administration. Gene Therapy 2007; 14: 1605-1609. (Pubitemid 350056232)
157. Yan Z, Zak R, Zhang Y, Ding W, Godwin S, Munson K et al. Distinct classes of proteasome-modulating agents cooperatively augment recombinant adeno-associated virus type 2 and type 5-mediated transduction from the apical surfaces of human airway epithelia. J Virol 2004; 78: 2863-2874. (Pubitemid 38314344)
158. Zhang T, Hu J, Ding W, Wang X. Doxorubicin augments rAAV-2 transduction in rat neuronal cells. Neurochem Int 2009; 55: 521-528.
159. Hansen J, Qing K, Srivastava A. Adeno-associated virus type 2-mediated gene transfer: altered endocytic processing enhances transduction efficiency in murine fibroblasts. J Virol 2001; 75: 4080-4090. (Pubitemid 32410120)
160. Ju XD, Lou SQ, Wang WG, Peng JQ, Tian H. Effect of hydroxyurea and etoposide on transduction of human bone marrow mesenchymal stem and progenitor cell by adeno-associated virus vectors. Acta Pharmacol Sin 2004; 25: 196-202. (Pubitemid 38186170)
161. Russell DW, Alexander IE, Miller AD. DNA synthesis and topoisomerase inhibitors increase transduction by adeno-associated virus vectors. Proc Natl Acad Sci USA 1995; 92: 5719-5723.
162. Qing K, Li W, Zhong L, Tan M, Hansen J, Weigel-Kelley KA et al. Adeno-associated virus type 2-mediated gene transfer: role of cellular T-cell protein tyrosine phosphatase in transgene expression in established cell lines in vitro and transgenic mice in vivo. J Virol 2003; 77: 2741-2746. (Pubitemid 36222799)
163. Zhong L, Li B, Mah C, 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 Natl Acad Sci USA 2008; 105: 7827-7832. (Pubitemid 351872723)
164. Kauss MA, Smith LJ, Zhong L, Srivastava A, Wong KK, Chatterjee S. Enhanced longterm 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.