Prolonged susceptibility to antibody-mediated neutralization for adeno-associated vectors targeted to the liver

Molecular Therapy

Volumn 16, Issue 1, 2008, Pages 138-145

  Murphy, Samuel L ^a   Li, Hojun ^a,b   Zhou, Shangzhen ^a   Schlachterman, Alexander ^a   High, Katherine ^a,c  

^a CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PARVOVIRUS VECTOR;

ADENO ASSOCIATED VIRUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; CELL ADHESION; CONTROLLED STUDY; ENDOCYTOSIS; GENE TRANSFER; HUMAN; HUMAN CELL; IN VIVO STUDY; LIVER CELL; MALE; MOUSE; NONHUMAN; VIRAL GENE DELIVERY SYSTEM; VIRUS ATTACHMENT; VIRUS NEUTRALIZATION;

ADENO-ASSOCIATED VIRUS; MUS;

EID: 37549003977     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/sj.mt.6300334     Document Type: Article

References (47)

1. Herzog, RW, Hagstrom, JN, Kung, SH, Tai, SJ, Wilson, JM, Fisher, KJ et al. (1997). Stable gene transfer and expression of human blood coagulation factor IX after intramuscular injection of recombinant adeno-associated virus. Proc Natl Acad Sci USA 94: 5804-5809.
2. High, K (2005). Gene transfer for hemophilia: Can therapeutic efficacy in large animals be safely translated to patients? J Thromb Haemost 3: 1682-1691.
3. Arruda, VR, Stedman, HH, Nichols, TC, Haskins, ME, Nicholson, M, Herzog, RW et al. (2005). Regional intravascular delivery of AAV-2-F.IX to skeletal muscle achieves long-term correction of hemophilia B in a large animal model. Blood 105: 3458-3464.
4. Mount, JD, Herzog, RW, Tillson, DM, Goodman, SA, Robinson, N, McCleland, ML et al. (2002). Sustained phenotypic correction of hemophilia B dogs with a factor IX null mutation by liver-directed gene therapy. Blood 99: 2670-2676.
5. Wang, L, Calcedo, R, Nichols, TC, Bellinger, DA, Dillow, A, Verma, IM et al. (2005). Sustained correction of disease in naive and AAV2-pretreated hemophilia B dogs: AAV2/8-mediated, liver-directed gene therapy. Blood 105: 3079-3086.
6. High, KA (2004). Clinical gene transfer studies for hemophilia B. Semin Thromb Hemost 30: 257-267.
7. Manno, CS, Pierce, GF, Arruda, VR, Glader, B, Ragni, M, Rasko, JJ et al. (2006). Successful transduction of liver in hemophilia by AAV-Factor IX and limitations imposed by the host immune response. Nat Med 12: 342-347.
8. Sun, JY, Chatterjee, S and Wong, KK Jr. (2002). Immunogenic issues concerning recombinant adeno-associated virus vectors for gene therapy. Curr Gene Ther 2: 485-500.
9. Grimm, D and Kay, MA (2003). 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 3: 281-304.
10. Moskalenko, M, Chen, L, van Roey, M, Donahue, BA, Snyder, RO, McArthur, JG et al. (2000). Epitope mapping of human anti-adeno-associated virus type 2 neutralizing antibodies: Implications for gene therapy and virus structure. J Virol 74: 1761-1766.
11. Jiang, H, Couto, LB, Patarroyo-White, S, Liu, T, Nagy, D, Vargas, JA et al. (2006). Effects of transient immunosuppression on adenoassociated, virus-mediated, liver-directed gene transfer in rhesus macaques and implications for human gene therapy. Blood 108: 3321-3328.
12. Scallan, CD, Jiang, H, Liu, T, Patarroyo-White, S, Sommer, JM, Zhou, S et al. (2006). Human immunoglobulin inhibits liver transduction by AAV vectors at low AAV2 neutralizing titers in SCID mice. Blood 107: 1810-1817.
13. Chirmule, N, Propert, K, Magosin, S, Qian, Y, Qian, R and Wlson, J (1999). Immune responses to adenovirus and adeno-associated virus in humans. Gene Ther 6: 1574-1583.
14. Erles, K, Sebokova, P and Schlehofer, JR (1999). Update on the prevalence of serum antibodies (IgG and IgM) to adeno-associated virus (AAV). J Med Virol 59: 406-411.
15. Blacklow, NR, Hoggan, MD, Sereno, MS, Brandt CD, Kim, HW, Parrott, RH et al. (1971). A seroepidemiologic study of adenovirus-associated virus infection in infants and children. Am J Epidemiol 94: 359-366.
16. Blacklow, NR, Hoggan, MD, Kapikian, AZ, Austin, JB and Rowe, WP (1968). Epidemiology of adenovirus-associated virus infection in a nursery population. Am J Epidemiol 88: 368-378.
17. Riviere, C, Danos, O and Douar, AM (2006). Long-term expression and repeated administration of AAV type 1, 2 and 5 vectors in skeletal muscle of immunocompetent adult mice. Gene Ther 13: 1300-1308.
18. Lochrie, MA, Tatsuno, GP, Christie, B, McDonnell, JW, Zhou, S, Surosky, R et al. (2006). Mutations on the external surfaces of adeno-associated virus type 2 capsids that affect transduction and neutralization. J Virol 80: 821-834.
19. Schaffer, DV and Maheshri, N (2004). Directed evolution of AAV mutants for enhanced gene delivery. Conf Proc IEEE Eng Med Biol Soc 5 3520-3523.
20. Muller, OJ, Kaul, F, Weitzman, MD, Pasqualini, R, Arap, W, Kleinschmidt, JA et al. (2003). Random peptide libraries displayed on adeno-associated virus to select for targeted gene therapy vectors. Nat Biotechnol 21: 1040-1046.
21. Maheshri, N, Koerber, JT, Kaspar, BK and Schaffer, DV (2006). Directed evolution of adeno-associated virus yields enhanced gene delivery vectors. Nat Biotechnol 24: 198-204.
22. Huttner, NA, Girod, A, Perabo, L, Edbauer, D, Kleinschmidt, A, Buning, H et al. (2003). Genetic modifications of the adeno-associated virus type 2 capsid reduce the affinity and the neutralizing effects of human serum antibodies. Gene Ther 10: 2139-2147.
23. Manning, WC, Zhou, S, Bland, MP, Escobedo, JA and Dwarki, V (1998). Transient immunosuppression allows transgene expression following readministration of adeno-associated viral vectors. Hum Gene Ther 9: 477-485.
24. Halbert, CL, Standaert, TA, Wilson, CB and Miller, AD (1998) Successful readministration of adeno-associated virus vectors to the mouse lung requires transient immunosuppression during the initial exposure. J Virol 72: 9795-9805.
25. Sarukhan, A, Camugli, S, Gjata, B, von Boehmer, H, Danos, O and Jooss, K (2001). Successful interference with cellular immune responses to immunogenic proteins encoded by recombinant viral vectors. J Virol 75: 269-277.
26. Chen, Y, Yu, DC, Charlton, D and Henderson, DR (2000). Pre-existent adenovirus antibody inhibits systemic toxicity and antitumor activity of CN706 in the nude mouse LNCaP xenograft model: Implications and proposals for human therapy. Hum Gene Ther 11: 1553-1567.
27. Hodges, BL, Taylor, KM, Chu, Q, Scull, SE, Serriello, RG, Anderson, SC et al. (2005). Local delivery of a viral vector mitigates neutralization by antiviral antibodies and results in efficient transduction of rabbit liver. Mol Ther 12: 1043-1051.
28. Ohashi, K, Nakai, H, Couto, LB and Kay, MA (2005). Modified infusion procedures affect recombinant adeno-associated virus vector type 2 transduction in the liver. Hum Gene Ther 16: 299-306.
29. Bartlett, JS, Wilcher, R and Samulski, RJ (2000). Infectious entry pathway of adeno-associated virus and adeno-associated virus vectors. J Virol 74: 2777-2785.
30. Pajusola, K, Gruchala, M, Joch, H, Luscher, TF, Yla-Herttuala, S and Bueler, H (2002). Cell-type-specific characteristics modulate the transduction efficiency of adeno-associated virus type 2 and restrain infection of endothelial cells. J Virol 76: 11530-11540.
31. Ding, W, Zhang, L, Yan, Z and Engelhardt, JF (2005). Intracellular trafficking of adeno-associated viral vectors. Gene Ther 12: 873-880.
32. Xiao, W, Warrington, KH Jr., Hearing, P, Hughes, J and Muzyczka, N (2002). Adenovirus-facilitated nuclear translocation of adeno-associated virus type 2. J Virol 76: 11505-11517.
33. Weinstein, R (1997). Basic prinicples of therapeutic blood exchange. In McCleod, BC (ed). Apheresis - Principles and Practice. AABB Press, Bethesda, pp. 263-286.
34. Gao, GP, Alvira, MR, Wang, L, Calcedo, R, Johnston, J and Wilson, JM (2002). Novel adeno-associated viruses from rhesus monkeys as vectors for human gene therapy. Proc Natl Acad Sci USA 99: 11854-11859.
35. Kern, A, Schmidt, K, Leder, C, Muller, OJ, Wobus, CE, Bettinger, K et al. (2003). Identification of a heparin-binding motif on adeno-associated virus type 2 capsids. J Virol 77: 11072-11081.
36. Wang, Z, Zhu, T, Qiao, C, Zhou, L, Wang, B, Zhang, J et al. (2005). Adeno-associated virus serotype 8 efficiently delivers genes to muscle and heart. Nat Biotechnol 23: 321-328.
37. Sanlioglu, AD, Karacay, B, Benson, PK, Engelhardt, JF and Sanlioglu, S (2004). Novel approaches to augment adeno-associated virus type-2 endocytosis and transduction. Virus Res 104: 51-59.
38. Duan, D, Li, Q, Kao, AW, Yue, Y, Pessin, JE and Engelhardt, JF (1999). Dynamin is required for recombinant adeno-associated virus type 2 infection. J Virol 73: 10371-10376.
39. Sanlioglu, S, Benson, P and Engelhardt, JF (2000). Loss of ATM function enhances recombinant adeno-associated virus transduction and integration through pathways similar to UV irradiation. Virology 268: 68-78.
40. Sanlioglu, S, Benson, PK, Yang, J, Atkinson, EM, Reynolds, T and Engelhardt, JF (2000). Endocytosis and nuclear trafficking of adeno-associated virus type 2 are controlled by rac1 and phosphatidylinositol-3 kinase activation. J Virol 74: 9184-9196.
41. Haim, H, Steiner, I and Panet, A (2007). Time frames for neutralization during the human immunodeficiency virus type 1 entry phase, as monitored in synchronously infected cell cultures. J Virol 81: 3525-3534.
42. Stone, D, Liu, Y, Shayakhmetov, D, Li, ZY, Ni, S and Lieber, A (2007). Adenovirus-platelet interaction in blood causes virus sequestration to the reticuloendothelial system of the liver. J Virol 81: 4866-4871.
43. Alemany, R, Suzuki, K and Curiel, DT (2000). Blood clearance rates of adenovirus type 5 in mice. J Gen Virol 81: 2605-2609.
44. Matsushita, T, Elliger, S, Elliger, C, Podsakoff, G, Villarreal, L, Kurtzman, GJ et al. (1998). Adeno-associated virus vectors can be efficiently produced without helper virus. Gene Ther 5: 938-945.
45. Nakai, H, Herzog, RW, Hagstrom, JN, Walter, J, Kung, SH, Yang, EY et al. (1998). Adeno-associated viral vector-mediated gene transfer of human blood coagulation factor IX into mouse liver. Blood 91 4600-4607.
46. Kung, SH, Hagstrom, JN, Cass, D, Tai, SJ, Lin, HF, Stafford, DW et al. (1998). Human factor IX corrects the bleeding diathesis of mice with hemophilia B. Blood 91: 784-790.
47. Walter, J You, Q Hagstrom, JN Sands, M and High, KA (1996). Successful expression of human factor IX following repeat administration of adenoviral vector in mice. Proc Natl Acad Sci USA 93: 3056-3061.