The pleiotropic effects of natural AAV infections on liver-directed gene transfer in macaques

Molecular Therapy

Volumn 18, Issue 1, 2010, Pages 126-134

  Wang, Lili ^a   Calcedo, Roberto ^b   Wang, Huan ^a,b   Bell, Peter ^a   Grant, Rebecca ^a   Vandenberghe, Luk H ^a   Sanmiguel, Julio ^a   Morizono, Hiroki ^c   Batshaw, Mark L ^c   Wilson, James M ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b SUN YAT SEN UNIVERSITY   (China)

^c GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; GREEN FLUORESCENT PROTEIN; NEUTRALIZING ANTIBODY; PARVOVIRUS VECTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; GENE EXPRESSION; GENE TRANSFER; IN VIVO GENE TRANSFER; LIVER CELL; LIVER DIRECTED GENE TRANSFER; MALE; MOUSE; NONHUMAN; PLEIOTROPY; RHESUS MONKEY; SEROTYPE; SPLEEN; TISSUE DISTRIBUTION; TRANSGENE; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY; VIRUS CAPSID;

ANIMALS; ANTIBODIES, NEUTRALIZING; DEPENDOVIRUS; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; LIVER; MACACA; TRANSDUCTION, GENETIC;

ANIMALIA; MACACA; MACACA MULATTA; MURINAE; PRIMATES;

EID: 74149088098     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2009.245     Document Type: Article

References (40)

1. Maguire, AM, Simonelli, F, Pierce, EA, Pugh, EN Jr, Mingozzi, F, Bennicelli, J et al. (2008). Safety and effcacy of gene transfer for Leber's congenital amaurosis. N Engl J Med 358: 2240-2248.
2. Bainbridge, JW, Smith, AJ, Barker, SS, Robbie, S, Henderson, R, Balaggan, K et al. (2008). Effect of gene therapy on visual function in Leber's congenital amaurosis. N Engl J Med 358: 2231-2239.
3. Hauswirth, WW, Aleman, TS, Kaushal, S, Cideciyan, AV, Schwartz, SB, Wang, L et al. (2008). Treatment of Leber congenital amaurosis due to RPE65 mutations by ocular subretinal injection of adeno-associated virus gene vector: short-term results of a phase I trial. Hum Gene Ther 19: 979-990.
4. Kaplitt, MG, Feigin, A, Tang, C, Fitzsimons, HL, Mattis, P, Lawlor, PA et al. (2007). Safety and tolerability of gene therapy with an adeno-associated virus (AAV) borne GAD gene for Parkinson's disease: an open label, phase I trial. Lancet 369: 2097-2105.
5. Eberling, JL, Jagust, WJ, Christine, CW, Starr, P, Larson, P, Bankiewicz, KS et al. (2008). Results from a phase I safety trial of hAADC gene therapy for Parkinson disease. Neurology 70: 1980-1983.
6. 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.
7. Mingozzi, F, Maus, MV, Hui, DJ, Sabatino, DE, Murphy, SL, Rasko, JE et al. (2007). CD8+ T-cell responses to adeno-associated virus capsid in humans. Nat Med 13: 419-422.
8. Snyder, RO, Miao, CH, Patijn, GA, Spratt, SK, Danos, O, Nagy, D et al. (1997). Persistent and therapeutic concentrations of human factor IX in mice after hepatic gene transfer of recombinant AAV vectors. Nat Genet 16: 270-276.
9. ash mice. Mol Ther 17: 1340-1346.
10. Gao, G, Wang, Q, Calcedo, R, Mays, L, Bell, P, Wang, L et al. (2009). AAV-mediated gene transfer to nonhuman primate liver can elicit destructive transgene-specifc T cell responses. Hum Gene Ther 20: 930-942.
11. Gao, G P, 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.
12. Gao, G, Alvira, MR, Somanathan, S, Lu, Y, Vandenberghe, LH, Rux, JJ et al. (2003). Adeno-associated viruses undergo substantial evolution in primates during natural infections. Proc Natl Acad Sci USA 100: 6081-6086.
13. Gao, G, Vandenberghe, LH, Alvira, MR, Lu, Y, Calcedo, R, Zhou, X et al. (2004). Clades of adeno-associated viruses are widely disseminated in human tissues. J Virol 78: 6381-6388.
14. Calcedo, R, Vandenberghe, LH, Gao, G, Lin, J and Wilson, JM (2009). Worldwide epidemiology of neutralizing antibodies to adeno-associated viruses. J Infect Dis 199: 381-390.
15. Murphy, SL, Li, H, Mingozzi, F, Sabatino, DE, Hui, DJ, Edmonson, SA et al. (2009). Diverse IgG subclass responses to adeno-associated virus infection and vector administration. J Med Virol 81: 65-74.
16. Vandenberghe, LH, Wang, L, Somanathan, S, Zhi, Y, Figueredo, J, Calcedo, R et al. (2006). Heparin binding directs activation of T cells against adeno-associated virus serotype 2 capsid. Nat Med 12: 967-971.
17. Wang, L, Wang, H, Bell, P, McCarter, RJ, He, J, Calcedo, R et al. (2009). Systematic evaluation of AAV vectors for liver-directed gene transfer in murine models. Mol Ther, this issue.
18. Cordier, L, Gao, GP, Hack, AA, McNally, EM, Wilson, JM, Chirmule, N et al. (2001). Muscle-specifc promoters may be necessary for adeno-associated virus-mediated gene transfer in the treatment of muscular dystrophies. Hum Gene Ther 12: 205-215.
19. Franco, LM, Sun, B, Yang, X, Bird, A, Zhang, H, Schneider, A et al. (2005). Evasion of immune responses to introduced human acid α-glucosidase by liver-restricted expression in glycogen storage disease type II. Mol Ther 12: 876-884.
20. Mori, S, Takeuchi, T and Kanda, T (2008). Antibody-dependent enhancement of adeno-associated virus infection of human monocytic cell lines. Virology 375: 141-147.
21. Ziegler, RJ, Lonning, SM, Armentano, D, Li, C, Souza, DW, Cherry, M et al. (2004). AAV2 vector harboring a liver-restricted promoter facilitates sustained expression of therapeutic levels of α-galactosidase A and the induction of immune tolerance in Fabry mice. Mol Ther 9: 231-240.
22. Brown, BD, Venneri, MA, Zingale, A, Sergi Sergi, L and Naldini, L (2006). Endogenous microRNA regulation suppresses transgene expression in hematopoietic lineages and enables stable gene transfer. Nat Med 12: 585-591.
23. Brown, BD, Cantore, A, Annoni, A, Sergi, LS, Lombardo, A, Della Valle, P et al. (2007). A microRNA-regulated lentiviral vector mediates stable correction of hemophilia B mice. Blood 110: 4144-4152.
24. Meier, O, Gastaldelli, M, Boucke, K, Hemmi, S and Greber, UF (2005). Early steps of clathrin-mediated endocytosis involved in phagosomal escape of Fcγ receptor-targeted adenovirus. J Virol 79: 2604-2613.
25. Clyde, K, Kyle, JL and Harris, E (2006). Recent advances in deciphering viral and host determinants of dengue virus replication and pathogenesis. J Virol 80: 11418-11431.
26. Munakata, Y, Kato, I, Saito, T, Kodera, T, Ishii, KK and Sasaki, T (2006). Human parvovirus B19 infection of monocytic cell line U937 and antibody-dependent enhancement. Virology 345: 251-257.
27. + T cell epitopes. Mol Ther 12: 1023-1033.
28. Chen, J, Wu, Q, Yang, P, Hsu, HC and Mountz, JD (2006). Determination of specifc CD4 and CD8 T cell epitopes after AAV2-and AAV8-hF.IX gene therapy. Mol Ther 13: 260-269.
29. Wang, L, Figueredo, J, Calcedo, R, Lin, J and Wilson, JM (2007). Cross-presentation of adeno-associated virus serotype 2 capsids activates cytotoxic T cells but does not render hepatocytes effective cytolytic targets. Hum Gene Ther 18: 185-194.
30. Li, C, Hirsch, M, Asokan, A, Zeithaml, B, Ma, H, Kafri, T et al. (2007). Adeno-associated virus type 2 (AAV2) capsid-specifc cytotoxic T lymphocytes eliminate only vector-transduced cells coexpressing the AAV2 capsid in vivo. J Virol 81: 7540-7547.
31. + T cells are unable to eliminate AAV-transduced hepatocytes. Mol Ther 15: 792-800.
32. Pien, GC, Basner-Tschakarjan, E, Hui, DJ, Mentlik, AN, Finn, JD, Hasbrouck, NC et al. (2009). Capsid antigen presentation fags human hepatocytes for destruction after transduction by adeno-associated viral vectors. J Clin Invest 119: 1688-1695.
33. Li, C, Goudy, K, Hirsch, M, Asokan, A, Fan, Y, Alexander, J et al. (2009). Cellular immune response to cryptic epitopes during therapeutic gene transfer. Proc Natl Acad Sci USA 106: 10770-10774.
34. Davidoff, AM, Gray, JT, Ng, CY, Zhang, Y, Zhou, J, Spence, Y et al. (2005). Comparison of the ability of adeno-associated viral vectors pseudotyped with serotype 2, 5, and 8 capsid proteins to mediate effcient transduction of the liver in murine and nonhuman primate models. Mol Ther 11: 875-888.
35. 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.
36. Gao, G, Lu, Y, Calcedo, R, Grant, RL, Bell, P, Wang, L et al. (2006). Biology of AAV serotype vectors in liver-directed gene transfer to nonhuman primates. Mol Ther 13: 77-87.
37. Vandenberghe, LH, Breous, E, Nam, HJ, Gao, G, Xiao, R, Sandhu, A et al. (2009). Naturally occurring singleton residues in AAV capsid impact vector performance and illustrate structural constraints. Gene Ther (epub ahead of print).
38. 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.
39. Calcedo, R, Vandenberghe, LH, Roy, S, Somanathan, S, Wang, L and Wilson, JM (2009). Host immune responses to chronic adenovirus infections in human and nonhuman primates. J Virol 83: 2623-2631.
40. Bell, P, Moscioni, AD, McCarter, RJ, Wu, D, Gao, G, Hoang, A et al. (2006). Analysis of tumors arising in male B6C3F1 mice with and without AAV vector delivery to liver. Mol Ther 14: 34-44.