Examining the cross-reactivity and neutralization mechanisms of a panel of mabs against adeno-associated virus serotypes 1 and 5

Journal of General Virology

Volumn 93, Issue 2, 2012, Pages

  Harbison, Carole E ^a   Weichert, Wendy S ^a   Gurda, Brittney L ^b   Chiorini, John A ^c   Agbandje McKenna, Mavis ^b   Parrish, Colin R ^a  

^a Department of Obstetrics Gynecology   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; IMMUNOGLOBULIN F(AB) FRAGMENT; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN M ANTIBODY; MONOCLONAL ANTIBODY; NEUTRALIZING ANTIBODY; PROTEIN VP1; PROTEIN VP2; PROTEIN VP3; VIRUS ANTIBODY;

ADENOVIRUS; ADENOVIRUS 1; ADENOVIRUS 5; ANTIBODY PRODUCTION; ARTICLE; CONTROLLED STUDY; CROSS REACTION; ENZYME LINKED IMMUNOSORBENT ASSAY; HEMAGGLUTINATION INHIBITION; HYBRIDOMA; IMMUNIZATION; IMMUNOGENICITY; IMMUNOHISTOCHEMISTRY; INHIBITION KINETICS; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN EXPRESSION; RECEPTOR BINDING; SEROTYPE; VIRAL GENE DELIVERY SYSTEM; VIRUS ATTACHMENT; VIRUS CAPSID; VIRUS LIKE AGENT; VIRUS NEUTRALIZATION; ADENO ASSOCIATED VIRUS; ANIMAL; IMMUNOLOGY; MOUSE; SERODIAGNOSIS;

ADENO-ASSOCIATED VIRUS; MIRIDAE; MUS;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; CROSS REACTIONS; DEPENDOVIRUS; IMMUNOGLOBULIN G; MICE; NEUTRALIZATION TESTS;

EID: 84855919646     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.035113-0     Document Type: Article

References (72)

1. Allocca, M., Tessitore, A., Cotugno, G. & Auricchio, A. (2006). AAVmediated gene transfer for retinal diseases. Expert Opin Biol Ther 6, 1279-1294.
2. Anderson, R., Macdonald, I., Corbett, T., Whiteway, A. & Prentice, H. G. (2000). A method for the preparation of highly purified adeno-associated virus using affinity column chromatography, protease digestion and solvent extraction. J Virol Methods 85, 23-34.
3. Boutin, S., Monteilhet, V., Veron, P., Leborgne, C., Benveniste, O., Montus, M. F. & Masurier, C. (2010). Prevalence of serum IgG and neutralizing factors against adeno-associated virus (AAV) types 1, 2, 5, 6, 8, and 9 in the healthy population: implications for gene therapy using AAV vectors. Hum Gene Ther 21, 704-712.
4. Breous, E., Somanathan, S., Bell, P. & Wilson, J. M. (2011). Inflammation promotes the loss of adeno-associated virus-mediated transgene expression in mouse liver. Gastroenterology 141, 348-357.e1-e3.
5. Burger, C., Gorbatyuk, O. S., Velardo, M. J., Peden, C. S., Williams, P., Zolotukhin, S., Reier, P. J., Mandel, R. J. & Muzyczka, N. (2004). Recombinant AAV viral vectors pseudotyped with viral capsids from serotypes 1, 2, and 5 display differential efficiency and cell tropism after delivery to different regions of the central nervous system. Mol Ther 10, 302-317.
6. Calcedo, R., Vandenberghe, L. H., Gao, G., Lin, J. & Wilson, J. M. (2009). Worldwide epidemiology of neutralizing antibodies to adenoassociated viruses. J Infect Dis 199, 381-390.
7. Chao, H., Liu, Y., Rabinowitz, J., Li, C., Samulski, R. J. & Walsh, C. E. (2000). Several log increase in therapeutic transgene delivery by distinct adeno-associated viral serotype vectors. Mol Ther 2, 619-623.
8. Conway, J. E., Rhys, C. M., Zolotukhin, I., Zolotukhin, S., Muzyczka, N., Hayward, G. S. & Byrne, B. J. (1999). High-titer recombinant adenoassociated virus production utilizing a recombinant herpes simplex virus type I vector expressing AAV-2 Rep and Cap. Gene Ther 6, 986-993.
9. Dai, J. & Rabie, A. B. (2007). The use of recombinant adenoassociated virus for skeletal gene therapy. Orthod Craniofac Res 10, 1-14.
10. Davidson, B. L., Stein, C. S., Heth, J. A., Martins, I., Kotin, R. M., Derksen, T. A., Zabner, J., Ghodsi, A. & Chiorini, J. A. (2000). 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 U S A 97, 3428-3432.
11. DiMattia, M., Govindasamy, L., Levy, H. C., Gurda-Whitaker, B., Kalina, A., Kohlbrenner, E., Chiorini, J. A., McKenna, R., Muzyczka, N. & other authors (2005). Production, purification, crystallization and preliminary X-ray structural studies of adeno-associated virus serotype 5. Acta Crystallogr Sect F Struct Biol Cryst Commun 61, 917-921.
12. Dimmock, N. J. (1993). Neutralization of animal viruses. Curr Top Microbiol Immunol 183, 1-149.
13. Di Pasquale, G., Davidson, B. L., Stein, C. S., Martins, I., Scudiero, D., Monks, A. & Chiorini, J. A. (2003). Identification of PDGFR as a receptor for AAV-5 transduction. Nat Med 9, 1306-1312.
14. Gao, G., Alvira, M. R., Somanathan, S., Lu, Y., Vandenberghe, L. H., Rux, J. J., Calcedo, R., Sanmiguel, J., Abbas, Z. & Wilson, J. M. (2003). Adeno-associated viruses undergo substantial evolution in primates during natural infections. Proc Natl Acad Sci U S A 100, 6081-6086.
15. Gao, G., Vandenberghe, L. H., Alvira, M. R., Lu, Y., Calcedo, R., Zhou, X. & Wilson, J. M. (2004). Clades of adeno-associated viruses are widely disseminated in human tissues. J Virol 78, 6381-6388.
16. Govindasamy, L., Padron, E., McKenna, R., Muzyczka, N., Kaludov, N., Chiorini, J. A. & Agbandje-McKenna, M. (2006). Structurally mapping the diverse phenotype of adeno-associated virus serotype 4. J Virol 80, 11556-11570.
17. Grieger, J. C. & Samulski, R. J. (2005). Adeno-associated virus as a gene therapy vector: vector development, production and clinical applications. Adv Biochem Eng Biotechnol 99, 119-145.
18. Grimm, D. & Kay, M. A. (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.
19. Hafenstein, S., Bowman, V. D., Sun, T., Nelson, C. D., Palermo, L. M., Chipman, P. R., Battisti, A. J., Parrish, C. R. & Rossmann, M. G. (2009). Structural comparison of different antibodies interacting with parvovirus capsids. J Virol 83, 5556-5566.
20. Halbert, C. L., Rutledge, E. A., Allen, J. M., Russell, D. W. & Miller, A. D. (2000). Repeat transduction in the mouse lung by using adenoassociated virus vectors with different serotypes. J Virol 74, 1524-1532.
21. Harbison, C. E., Lyi, S. M., Weichert, W. S. & Parrish, C. R. (2009). Early steps in cell infection by parvoviruses: host-specific differences in cell receptor binding but similar endosomal trafficking. J Virol 83, 10504-10514.
22. Hernandez, Y. J., Wang, J., Kearns, W. G., Loiler, S., Poirier, A. & Flotte, T. R. (1999). Latent adeno-associated virus infection elicits humoral but not cell-mediated immune responses in a nonhuman primate model. J Virol 73, 8549-8558.
23. Huttner, N. A., Girod, A., Perabo, L., Edbauer, D., Kleinschmidt, J. A., Büning, H. & Hallek, M. (2003). Genetic modifications of the adenoassociated virus type 2 capsid reduce the affinity and the neutralizing effects of human serum antibodies. Gene Ther 10, 2139-2147.
24. Johnson, J. S., Li, C., DiPrimio, N., Weinberg, M. S., McCown, T. J. & Samulski, R. J. (2010). 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 84, 8888-8902.
25. Kaludov, N., Brown, K. E., Walters, R. W., Zabner, J. & Chiorini, J. A. (2001). 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 75, 6884-6893.
26. Kerr, J. R., Cotmore, S. F., Bloom, M. E., Linden, R. M. & Parrish, C. R. (2006). Parvoviruses. London: Hodder Arnold.
27. Klasse, P. J. & Sattentau, Q. J. (2001). Mechanisms of virus neutralization by antibody. Curr Top Microbiol Immunol 260, 87-108.
28. Klasse, P. J. & Sattentau, Q. J. (2002). Occupancy and mechanism in antibody-mediated neutralization of animal viruses. J Gen Virol 83, 2091-2108.
29. Kuck, D., Kern, A. & Kleinschmidt, J. A. (2007). Development of AAV serotype-specific ELISAs using novel monoclonal antibodies. J Virol Methods 140, 17-24.
30. Law, M. & Hangartner, L. (2008). Antibodies against viruses: passive and active immunization. Curr Opin Immunol 20, 486-492.
31. Lerch, T. F., Xie, Q. & Chapman, M. S. (2010). The structure of adenoassociated virus serotype 3B (AAV-3B): insights into receptor binding and immune evasion. Virology 403, 26-36.
32. Li, Q., Miller, R., Han, P. Y., Pang, J., Dinculescu, A., Chiodo, V. & Hauswirth, W. W. (2008). Intraocular route of AAV2 vector administration defines humoral immune response and therapeutic potential. Mol Vis 14, 1760-1769.
33. Lin, J., Calcedo, R., Vandenberghe, L. H., Figueredo, J. M. & Wilson, J. M. (2008). Impact of preexisting vector immunity on the efficacy of adeno-associated virus-based HIV-1 Gag vaccines. Hum Gene Ther 19, 663-669.
34. Lochrie, M. A., Tatsuno, G. P., Christie, B., McDonnell, J. W., Zhou, S., Surosky, R., Pierce, G. F. & Colosi, P. (2006). Mutations on the external surfaces of adeno-associated virus type 2 capsids that affect transduction and neutralization. J Virol 80, 821-834.
35. López-Bueno, A., Mateu, M. G. & Almendral, J. M. (2003). High mutant frequency in populations of a DNA virus allows evasion from antibody therapy in an immunodeficient host. J Virol 77, 2701-2708.
36. Lorain, S., Gross, D. A., Goyenvalle, A., Danos, O., Davoust, J. & Garcia, L. (2008). Transient immunomodulation allows repeated injections of AAV1 and correction of muscular dystrophy in multiple muscles. Mol Ther 16, 541-547.
37. Maersch, S., Huber, A., Büning, H., Hallek, M. & Perabo, L. (2010). Optimization of stealth adeno-associated virus vectors by randomization of immunogenic epitopes. Virology 397, 167-175.
38. Maguire, A. M., Simonelli, F., Pierce, E. A., Pugh, E. N., Jr, Mingozzi, F., Bennicelli, J., Banfi, S., Marshall, K. A., Testa, F. & other authors (2008). Safety and efficacy of gene transfer for Leber's congenital amaurosis. N Engl J Med 358, 2240-2248.
39. Mallery, D. L., McEwan, W. A., Bidgood, S. R., Towers, G. J., Johnson, C. M. & James, L. C. (2010). Antibodies mediate intracellular immunity through tripartite motif-containing 21 (TRIM21). Proc Natl Acad Sci U S A 107, 19985-19990.
40. Marks, W. J., Jr, Bartus, R. T., Siffert, J., Davis, C. S., Lozano, A., Boulis, N., Vitek, J., Stacy, M., Turner, D. & Verhagen, L. (2010). Gene delivery of AAV2-neurturin for Parkinson's disease: a double-blind, randomised, controlled trial. Lancet Neurol 9, 1164-1172.
41. Michelfelder, S. & Trepel, M. (2009). Adeno-associated viral vectors and their redirection to cell-type specific receptors. Adv Genet 67, 29-60.
42. Miller, E. B., Gurda-Whitaker, B., Govindasamy, L., McKenna, R., Zolotukhin, S., Muzyczka, N. & Agbandje-McKenna, M. (2006). Production, purification and preliminary X-ray crystallographic studies of adeno-associated virus serotype 1. Acta Crystallogr Sect F Struct Biol Cryst Commun 62, 1271-1274.
43. Mingozzi, F. & High, K. A. (2011). Immune responses to AAV in clinical trials. Curr Gene Ther 11, 321-330.
44. Monteilhet, V., Saheb, S., Boutin, S., Leborgne, C., Veron, P., Montus, M. F., Moullier, P., Benveniste, O. & Masurier, C. (2011). A 10 patient case report on the impact of plasmapheresis upon neutralizing factors against adeno-associated virus (AAV) types 1, 2, 6, and 8. Mol Ther 19, 2084-2091.
45. Moskalenko, M., Chen, L., van Roey, M., Donahue, B. A., Snyder, R. O., McArthur, J. G. & Patel, S. D. (2000). Epitope mapping of human antiadeno-associated virus type 2 neutralizing antibodies: implications for gene therapy and virus structure. J Virol 74, 1761-1766.
46. Mueller, C. & Flotte, T. R. (2008). Clinical gene therapy using recombinant adeno-associated virus vectors. Gene Ther 15, 858-863.
47. Murphy, S. L., Li, H., Mingozzi, F., Sabatino, D. E., Hui, D. J., Edmonson, S. A. & High, K. A. (2009). Diverse IgG subclass responses to adeno-associated virus infection and vector administration. J Med Virol 81, 65-74.
48. Nam, H. J., Lane, M. D., Padron, E., Gurda, B., McKenna, R., Kohlbrenner, E., Aslanidi, G., Byrne, B., Muzyczka, N. & other authors (2007). Structure of adeno-associated virus serotype 8, a gene therapy vector. J Virol 81, 12260-12271.
49. Ng, R., Govindasamy, L., Gurda, B. L., McKenna, R., Kozyreva, O. G., Samulski, R. J., Parent, K. N., Baker, T. S. & Agbandje-McKenna, M. (2010). Structural characterization of the dual glycan binding adenoassociated virus serotype 6. J Virol 84, 12945-12957.
50. Parren, P. W. & Burton, D. R. (2001). The antiviral activity of antibodies in vitro and in vivo. Adv Immunol 77, 195-262.
51. Parrish, C. R. & Carmichael, L. E. (1983). Antigenic structure and variation of canine parvovirus type-2, feline panleukopenia virus, and mink enteritis virus. Virology 129, 401-414.
52. Petry, H., Brooks, A., Orme, A., Wang, P., Liu, P., Xie, J., Kretschmer, P., Qian, H. S., Hermiston, T. W. & Harkins, R. N. (2008). Effect of viral dose on neutralizing antibody response and transgene expression after AAV1 vector re-administration in mice. Gene Ther 15, 54-60.
53. Pierson, T. C., Fremont, D. H., Kuhn, R. J. & Diamond, M. S. (2008). Structural insights into the mechanisms of antibody-mediated neutralization of flavivirus infection: implications for vaccine development. Cell Host Microbe 4, 229-238.
54. Sabo, M. C., Luca, V., Prentoe, J., Hopcraft, S. E., Blight, K. J., Yi, M., Lemon, S. M., Ball, J. K., Bukh, J. & other authors (2011). Neutralizing monoclonal antibodies against hepatitis C virus E2 protein bind discontinuous epitopes and inhibit infection at a postattachment step. J Virol 85, 7005-7019.
55. Scallan, C. D., Lillicrap, D., Jiang, H., Qian, X., Patarroyo-White, S. L., Parker, A. E., Liu, T., Vargas, J., Nagy, D. & other authors (2003). Sustained phenotypic correction of canine hemophilia A using an adeno-associated viral vector. Blood 102, 2031-2037.
56. Strassheim, M. L., Gruenberg, A., Veijalainen, P., Sgro, J.-Y. & Parrish, C. R. (1994). Two dominant neutralizing antigenic determinants of canine parvovirus are found on the threefold spike of the virus capsid. Virology 198, 175-184.
57. Sui, J., Li, W., Murakami, A., Tamin, A., Matthews, L. J., Wong, S. K., Moore, M. J., Tallarico, A. S., Olurinde, M. & other authors (2004). Potent neutralization of severe acute respiratory syndrome (SARS) coronavirus by a human mAb to S1 protein that blocks receptor association. Proc Natl Acad Sci U S A 101, 2536-2541.
58. Sun, J. Y., Anand-Jawa, V., Chatterjee, S. & Wong, K. K. (2003). Immune responses to adeno-associated virus and its recombinant vectors. Gene Ther 10, 964-976.
59. Urabe, M., Ding, C. & Kotin, R. M. (2002). Insect cells as a factory to produce adeno-associated virus type 2 vectors. Hum Gene Ther 13, 1935-1943.
60. van der Marel, S., Comijn, E. M., Verspaget, H. W., van Deventer, S., van den Brink, G. R., Petry, H., Hommes, D. W. & Ferreira, V. (2011). Neutralizing antibodies against adeno-associated viruses in inflammatory bowel disease patients: implications for gene therapy. Inflamm Bowel Dis 17, 2436-2442.
61. Van Vliet, K. M., Blouin, V., Brument, N., Agbandje-McKenna, M. & Snyder, R. O. (2008). The role of the adeno-associated virus capsid in gene transfer. Methods Mol Biol 437, 51-91.
62. Walters, R. W., Yi, S. M., Keshavjee, S., Brown, K. E., Welsh, M. J., Chiorini, J. A. & Zabner, J. (2001). Binding of adeno-associated virus type 5 to 2,3-linked sialic acid is required for gene transfer. J Biol Chem 276, 20610-20616.
63. Willey, S. & Aasa-Chapman, M. M. (2008). Humoral immunity to HIV-1: neutralisation and antibody effector functions. Trends Microbiol 16, 596-604.
64. Wistuba, A., Kern, A., Weger, S., Grimm, D. & Kleinschmidt, J. A. (1997). Subcellular compartmentalization of adeno-associated virus type 2 assembly. J Virol 71, 1341-1352.
65. Wobus, C. E., Hügle-Dörr, B., Girod, A., Petersen, G., Hallek, M. & Kleinschmidt, J. A. (2000). Monoclonal antibodies against the adenoassociated virus type 2 (AAV-2) capsid: epitope mapping and identification of capsid domains involved in AAV-2-cell interaction and neutralization of AAV-2 infection. J Virol 74, 9281-9293.
66. Wu, Z., Asokan, A., Grieger, J. C., Govindasamy, L., Agbandje-McKenna, M. & Samulski, R. J. (2006a). Single amino acid changes can influence titer, heparin binding, and tissue tropism in different adeno-associated virus serotypes. J Virol 80, 11393-11397.
67. Wu, Z., Asokan, A. & Samulski, R. J. (2006b). Adeno-associated virus serotypes: vector toolkit for human gene therapy. Mol Ther 14, 316-327.
68. Wu, Z., Miller, E., Agbandje-McKenna, M. & Samulski, R. J. (2006c). a2,3 and a2,6 N-linked sialic acids facilitate efficient binding and transduction by adeno-associated virus types 1 and 6. J Virol 80, 9093-9103.
69. Xiao, W., Chirmule, N., Berta, S. C., McCullough, B., Gao, G. & Wilson, J. M. (1999). Gene therapy vectors based on adeno-associated virus type 1. J Virol 73, 3994-4003.
70. Zabner, J., Seiler, M., Walters, R., Kotin, R. M., Fulgeras, W., Davidson, B. L. & Chiorini, J. A. (2000). Adeno-associated virus type 5 (AAV5) but not AAV2 binds to the apical surfaces of airway epithelia and facilitates gene transfer. J Virol 74, 3852-3858.
71. Zaiss, A. K. & Muruve, D. A. (2008). Immunity to adeno-associated virus vectors in animals and humans: a continued challenge. Gene Ther 15, 808-816.
72. Zhong, L., Li, W., Li, Y., Zhao, W., Wu, J., Li, B., Maina, N., Bischof, D., Qing, K. & other authors (2006). 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.