Inhibition of antigen presentation during AAV gene therapy using virus peptides

Human Molecular Genetics

Volumn 27, Issue 4, 2018, Pages 601-613

  Shao, Wenwei ^a   Chen, Xiaojing ^a   Samulski, Richard J ^a   Hirsch, Matthew L ^a   Li, Chengwen ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

ADENO ASSOCIATED VIRUS VECTOR; CD69 ANTIGEN; CD8 ANTIGEN; FURIN; GAMMA INTERFERON; HYBRID PROTEIN; MINI DYSTROPHIN ICP47 FUSION PROTEIN; OVALBUMIN; PEPTIDE; UNCLASSIFIED DRUG; US6 PEPTIDE; VIRAL PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTATION; ARTICLE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOTOXIC LYMPHOCYTE; CYTOTOXICITY; DRUG POTENCY; DUCHENNE MUSCULAR DYSTROPHY; HEK293 CELL LINE; HUMAN; HUMAN CELL; IMMUNOSUPPRESSIVE TREATMENT; MDCK CELL LINE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RAT; T LYMPHOCYTE ACTIVATION; VIRAL GENE THERAPY; ANIMAL; DEPENDOPARVOVIRUS; FEMALE; GENE THERAPY; GENETICS; IMMUNOLOGY; MALE; METABOLISM; PROCEDURES; SKELETAL MUSCLE; SPLEEN; T LYMPHOCYTE;

ANIMALS; ANTIGEN PRESENTATION; DEPENDOVIRUS; FEMALE; GENETIC THERAPY; MALE; MICE; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, DUCHENNE; PEPTIDES; SPLEEN; T-LYMPHOCYTES; VIRAL PROTEINS;

EID: 85041541012     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddx427     Document Type: Article

References (90)

1. DeSilva, S., Drachman, D.B., Mellits, D. and Kuncl, R.W. (1987) Prednisone treatment in Duchenne muscular dystrophy. Long-termbenefit. Arch. Neurol., 44, 818-822.
2. Blankinship, M.J., Gregorevic, P. and Chamberlain, J.S. (2006) Gene therapy strategies for Duchenne muscular dystrophy utilizing recombinant adeno-associated virus vectors. Mol. Ther., 13, 241-249.
3. Bostick, B., Yue, Y., Lai, Y., Long, C., Li, D. and Duan, D. (2008) Adeno-associated virus serotype-9 microdystrophin gene therapy ameliorates electrocardiographic abnormalities in mdx mice. Hum. Gene. Ther., 19, 851-856.
4. Denti, M.A., Rosa, A., D'Antona, G., Sthandier, O., De Angelis, F.G., Nicoletti, C., Allocca, M., Pansarasa, O., Parente, V., Musaro, A. et al. (2006) Body-wide gene therapy of Duchenne muscular dystrophy in the mdx mouse model. Proc. Natl. Acad. Sci. U S A, 103, 3758-3763.
5. Ghosh, A., Yue, Y., Long, C., Bostick, B. and Duan, D. (2007) Efficient whole-body transduction with trans-splicing adeno-associated viral vectors. Mol. Ther., 15, 750-755.
6. Ghosh, A., Yue, Y., Shin, J.H. and Duan, D. (2009) Systemic Trans-splicing adeno-associated viral delivery efficiently transduces the heart of adult mdx mouse, a model for duchenne muscular dystrophy. Hum. Gene. Ther., 20, 1319-1328.
7. Goncalves, M.A., van Nierop, G.P., Tijssen, M.R., Lefesvre, P., Knaan-Shanzer, S., van der Velde, I., van Bekkum, D.W., Valerio, D. and de Vries, A.A. (2005) Transfer of the full-length dystrophin-coding sequence into muscle cells by a dual high-capacity hybrid viral vector with site-specific integration ability. J. Virol., 79, 3146-3162.
8. Judge, L.M. and Chamberlain, J.S. (2005) Gene therapy for Duchenne muscular dystrophy: AAV leads the way. Acta Myol., 24, 184-193.
9. Lai, Y., Yue, Y. and Duan, D. (2010) Evidence for the failure of adeno-associated virus serotype 5 to package a viral genome > or=8.2 kb. Mol. Ther., 18, 75-79.
10. Lorain, S., Gross, D.A., Goyenvalle, A., Danos, O., Davoust, J. and Garcia, L. (2008) Transient immunomodulation allows repeated injections of AAV1 and correction of muscular dystrophy in multiple muscles. Mol. Ther., 16, 541-547.
11. Percival, J.M., Gregorevic, P., Odom, G.L., Banks, G.B., Chamberlain, J.S. and Froehner, S.C. (2007) rAAV6-microdystrophin rescues aberrant Golgi complex organization in mdx skeletal muscles. Traffic, 8, 1424-1439.
12. Townsend, D., Blankinship, M.J., Allen, J.M., Gregorevic, P., Chamberlain, J.S. and Metzger, J.M. (2007) Systemic administration of micro-dystrophin restores cardiac geometry and prevents dobutamine-induced cardiac pump failure. Mol. Ther., 15, 1086-1092.
13. Wang, B., Li, J., Fu, F.H. and Xiao, X. (2009) Systemic human minidystrophin gene transfer improves functions and life span of dystrophin and dystrophin/utrophin-deficient mice. J. Orthop. Res., 27, 421-426.
14. Wang, Z., Kuhr, C.S., Allen, J.M., Blankinship, M., Gregorevic, P., Chamberlain, J.S., Tapscott, S.J. and Storb, R. (2007) Sustained AAV-mediated dystrophin expression in a canine model of Duchenne muscular dystrophy with a brief course of immunosuppression. Mol. Ther., 15, 1160-1166.
15. Wang, B., Li, J. and Xiao, X. (2000) Adeno-associated virus vector carrying human minidystrophin genes effectively ameliorates muscular dystrophy in mdx mouse model. Proc. Natl. Acad. Sci. U S A, 97, 13714-13719.
16. Yuasa, K., Yoshimura, M., Urasawa, N., Ohshima, S., Howell, J.M., Nakamura, A., Hijikata, T., Miyagoe-Suzuki, Y. and Takeda, S. (2007) Injection of a recombinant AAV serotype 2 into canine skeletal muscles evokes strong immune responses against transgene products. Gene. Ther., 14, 1249-1260.
17. Yue, Y., Li, Z., Harper, S.Q., Davisson, R.L., Chamberlain, J.S. and Duan, D. (2003) Microdystrophin gene therapy of cardiomyopathy restores dystrophin-glycoprotein complex and improves sarcolemma integrity in the mdx mouse heart. Circulation, 108, 1626-1632.
18. Chamberlain, J.R. and Chamberlain, J.S. (2017) Progress toward Gene Therapy for Duchenne Muscular Dystrophy. Mol. Ther., 25, 1125-1131.
19. Bengtsson, N.E., Hall, J.K., Odom, G.L., Phelps, M.P., Andrus, C.R., Hawkins, R.D., Hauschka, S.D., Chamberlain, J.R. and Chamberlain, J.S. (2017) Muscle-specific CRISPR/Cas9 dystrophin gene editing ameliorates pathophysiology in a mouse model for Duchenne muscular dystrophy. Nat. Commun., 8, 14454.
20. Tabebordbar, M., Zhu, K., Cheng, J.K.W., Chew, W.L., Widrick, J.J., Yan, W.X., Maesner, C., Wu, E.Y., Xiao, R., Ran, F.A. et al. (2016) In vivo gene editing in dystrophic mouse muscle and muscle stem cells. Science, 351, 407-411.
21. Nelson, C.E., Hakim, C.H., Ousterout, D.G., Thakore, P.I., Moreb, E.A., Rivera, R.M.C., Madhavan, S., Pan, X., Ran, F.A., Yan, W.X. et al. (2016) In vivo genome editing improves muscle function in a mouse model of Duchenne muscular dystrophy. Science, 351, 403-407.
22. Long, C., Amoasii, L., Mireault, A.A., McAnally, J.R., Li, H., Sanchez-Ortiz, E., Bhattacharyya, S., Shelton, J.M., Bassel- Duby, R. and Olson, E.N. (2016) Postnatal genome editing partially restores dystrophin expression in a mouse model of muscular dystrophy. Science, 351, 400-403.
23. Yue, Y., Pan, X., Hakim, C.H., Kodippili, K., Zhang, K., Shin, J.H., Yang, H.T., McDonald, T. and Duan, D. (2015) Safe and bodywide muscle transduction in young adult Duchenne muscular dystrophy dogs with adeno-associated virus. Hum. Mol. Genet., 24, 5880-5890.
24. Kawecka, K., Theodoulides, M., Hasoglu, Y., Jarmin, S., Kymalainen, H., Le-Heron, A., Popplewell, L., Malerba, A., Dickson, G. and Athanasopoulos, T. (2015) Adeno-associated virus (AAV) mediated dystrophin gene transfer studies and exon skipping strategies for Duchenne muscular dystrophy (DMD). Curr. Gene Ther., 15, 395-415.
25. Le Guiner, C., Montus, M., Servais, L., Cherel, Y., Francois, V., Thibaud, J.L., Wary, C., Matot, B., Larcher, T., Guigand, L. et al. (2014) Forelimb treatment in a large cohort of dystrophic dogs supports delivery of a recombinant AAV for exon skipping in Duchenne patients. Mol. Ther., 22, 1923-1935.
26. Shin, J.H., Pan, X., Hakim, C.H., Yang, H.T., Yue, Y., Zhang, K., Terjung, R.L. and Duan, D. (2013) Microdystrophin ameliorates muscular dystrophy in the canine model of duchenne muscular dystrophy. Mol. Ther., 21, 750-757.
27. Wang, Z., Storb, R., Halbert, C.L., Banks, G.B., Butts, T.M., Finn, E.E., Allen, J.M., Miller, A.D., Chamberlain, J.S. and Tapscott, S.J. (2012) Successful regional delivery and long-term expression of a dystrophin gene in canine muscular dystrophy: a preclinical model for human therapies. Mol. Ther., 20, 1501-1507.
28. Shin, J.H., Yue, Y., Srivastava, A., Smith, B., Lai, Y. and Duan, D. (2012) A simplified immune suppression scheme leads to persistent micro-dystrophin expression in Duchenne muscular dystrophy dogs. Hum. Gene. Ther., 23, 202-209.
29. Bowles, D.E., McPhee, S.W., Li, C., Gray, S.J., Samulski, J.J., Camp, A.S., Li, J., Wang, B., Monahan, P.E., Rabinowitz, J.E. et al. (2012) Phase 1 gene therapy for Duchenne muscular dystrophy using a translational optimized AAV vector. Mol. Ther., 20, 443-455.
30. Li, C., Bowles, D.E., van Dyke, T. and Samulski, R.J. (2005) Adeno-associated virus vectors: potential applications for cancer gene therapy. Cancer. Gene. Ther., 12, 913-925.
31. Wang, Z., Zhu, T., Qiao, C., Zhou, L., Wang, B., Zhang, J., Chen, C., Li, J. and Xiao, X. (2005) Adeno-associated virus serotype 8 efficiently delivers genes to muscle and heart. Nat. Biotechnol., 23, 321-328.
32. Blankinship, M.J., Gregorevic, P., Allen, J.M., Harper, S.Q., Harper, H., Halbert, C.L., Miller, A.D. and Chamberlain, J.S. (2004) Efficient transduction of skeletal muscle using vectors based on adeno-associated virus serotype 6. Mol. Ther., 10, 671-678.
33. Odom, G.L., Gregorevic, P., Allen, J.M., Finn, E. and Chamberlain, J.S. (2008) Microutrophin delivery through rAAV6 increases lifespan and improves muscle function in dystrophic dystrophin/utrophin-deficient mice. Mol. Ther., 16, 1539-1545.
34. Mendell, J.R., Campbell, K., Rodino-Klapac, L., Sahenk, Z., Shilling, C., Lewis, S., Bowles, D., Gray, S., Li, C., Galloway, G. et al. (2010) Dystrophin immunity in Duchenne's muscular dystrophy. N. Engl. J. Med., 363, 1429-1437.
35. Fanin, M., Danieli, G.A., Cadaldini, M., Miorin, M., Vitiello, L. and Angelini, C. (1995) Dystrophin-positive fibers in Duchenne dystrophy: origin and correlation to clinical course. Muscle Nerve, 18, 1115-1120.
36. Burrow, K.L., Coovert, D.D., Klein, C.J., Bulman, D.E., Kissel, J.T., Rammohan, K.W., Burghes, A.H. and Mendell, J.R. CIDD Study Group (1991) Dystrophin expression and somatic reversion in prednisone-treated and untreated Duchenne dystrophy. Neurology, 41, 661-666.
37. Uchino, M., Tokunaga, M., Mita, S., Uyama, E., Ando, Y., Teramoto, H., Miike, T. and Ando, M. (1995) PCR and immunocytochemical analyses of dystrophin-positive fibers in Duchenne muscular dystrophy. J. Neurol. Sci., 129, 44-50.
38. Hoffman, E.P., Morgan, J.E., Watkins, S.C. and Partridge, T.A. (1990) Somatic reversion/suppression of the mouse mdx phenotype in vivo. J. Neurol. Sci., 99, 9-25.
39. Crawford, G.E., Lu, Q.L., Partridge, T.A. and Chamberlain, J.S. (2001) Suppression of revertant fibers in mdx mice by expression of a functional dystrophin. Hum. Mol. Genet., 10, 2745-2750.
40. Sicinski, P., Geng, Y., Ryder-Cook, A.S., Barnard, E.A., Darlison, M.G. and Barnard, P.J. (1989) The molecular basis of muscular dystrophy in the mdx mouse: a point mutation. Science, 244, 1578-1580.
41. Wilton, S.D., Dye, D.E., Blechynden, L.M. and Laing, N.G. (1997) Revertant fibres: a possible genetic therapy for Duchenne muscular dystrophy?. Neuromuscul. Disord., 7, 329-335.
42. Valentine, B.A., Winand, N.J., Pradhan, D., Moise, N.S., de Lahunta, A., Kornegay, J.N. and Cooper, B.J. (1992) Canine X-linked muscular dystrophy as an animal model of Duchenne muscular dystrophy: a review. Am. J. Med. Genet., 42, 352-356.
43. Lybarger, L., Wang, X., Harris, M. and Hansen, T.H. (2005) Viral immune evasion molecules attack the ER peptide-loading complex and exploit ER-associated degradation pathways. Curr. Opin. Immunol., 17, 71-78.
44. Seliger, B., Ritz, U. and Ferrone, S. (2006) Molecular mechanisms of HLA class I antigen abnormalities following viral infection and transformation. Int. J. Cancer, 118, 129-138.
45. Lilley, B.N. and Ploegh, H.L. (2005) Viral modulation of antigen presentation: manipulation of cellular targets in the ER and beyond. Immunol. Rev., 207, 126-144.
46. Ambagala, A.P., Solheim, J.C. and Srikumaran, S. (2005) Viral interference with MHC class I antigen presentation pathway: the battle continues. Vet. Immunol. Immunopathol., 107, 1-15.
47. Ahn, K., Angulo, A., Ghazal, P., Peterson, P.A., Yang, Y. and Fruh, K. (1996) Human cytomegalovirus inhibits antigen presentation by a sequential multistep process. Proc. Natl. Acad. Sci. U S A, 93, 10990-10995.
48. Ahn, K., Gruhler, A., Galocha, B., Jones, T.R., Wiertz, E.J., Ploegh, H.L., Peterson, P.A., Yang, Y. and Fruh, K. (1997) The ER-luminal domain of the HCMV glycoprotein US6 inhibits peptide translocation by TAP. Immunity, 6, 613-621.
49. Ahn, K., Meyer, T.H., Uebel, S., Sempe, P., Djaballah, H., Yang, Y., Peterson, P.A., Fruh, K. and Tampe, R. (1996) Molecular mechanism and species specificity of TAP inhibition by herpes simplex virus ICP47. Embo. J., 15, 3247-3255.
50. Hengel, H., Koopmann, J.O., Flohr, T., Muranyi, W., Goulmy, E., Hammerling, G.J., Koszinowski, U.H. and Momburg, F. (1997) A viral ER-resident glycoprotein inactivates the MHC-encoded peptide transporter. Immunity, 6, 623-632.
51. Hengel, H., Reusch, U., Gutermann, A., Ziegler, H., Jonjic, S., Lucin, P. and Koszinowski, U.H. (1999) Cytomegaloviral control of MHC class I function in the mouse. Immunol. Rev., 168, 167-176.
52. Lehner, P.J., Karttunen, J.T., Wilkinson, G.W. and Cresswell, P. (1997) The human cytomegalovirus US6 glycoprotein inhibits transporter associated with antigen processingdependent peptide translocation. Proc. Natl. Acad. Sci. U S A, 94, 6904-6909.
53. York, I.A., Roop, C., Andrews, D.W., Riddell, S.R., Graham, F.L. and Johnson, D.C. (1994) A cytosolic herpes simplex virus protein inhibits antigen presentation to CD8+ T lymphocytes. Cell, 77, 525-535.
54. Fruh, K., Ahn, K., Djaballah, H., Sempe, P., van Endert, P.M., Tampe, R., Peterson, P.A. and Yang, Y. (1995) A viral inhibitor of peptide transporters for antigen presentation. Nature, 375, 415-418.
55. Hill, A., Jugovic, P., York, I., Russ, G., Bennink, J., Yewdell, J., Ploegh, H. and Johnson, D. (1995) Herpes simplex virus turns offthe TAP to evade host immunity. Nature, 375, 411-415.
56. Tomazin, R., Hill, A.B., Jugovic, P., York, I., van Endert, P., Ploegh, H.L., Andrews, D.W. and Johnson, D.C. (1996) Stable binding of the herpes simplex virus ICP47 protein to the peptide binding site of TAP. Embo. J., 15, 3256-3266.
57. Tomazin, R., van Schoot, N.E., Goldsmith, K., Jugovic, P., Sempe, P., Fruh, K. and Johnson, D.C. (1998) Herpes simplex virus type 2 ICP47 inhibits human TAP but not mouse TAP. J. Virol., 72, 2560-2563.
58. Hirsch, M.L., Li, C., Bellon, I., Yin, C., Chavala, S., Pryadkina, M., Richard, I. and Samulski, R.J. (2013) Oversized AAV transductifon is mediated via a DNA-PKcs-independent, Rad51C-dependent repair pathway. Mol. Ther., 21, 2205-2216.
59. Mays, L.E., Vandenberghe, L.H., Xiao, R., Bell, P., Nam, H.J., Agbandje-McKenna, M. and Wilson, J.M. (2009) Adeno-associated virus capsid structure drives CD4-dependent CD8+ T cell response to vector encoded proteins. J. Immunol., 182, 6051-6060.
60. Lin, S.W., Hensley, S.E., Tatsis, N., Lasaro, M.O. and Ertl, H.C. (2007) Recombinant adeno-associated virus vectors induce functionally impaired transgene product-specific CD8+ T cells in mice. J. Clin. Invest., 117, 3958-3970.
61. Mays, L.E., Wang, L., Lin, J., Bell, P., Crawford, A., Wherry, E.J. and Wilson, J.M. (2014) AAV8 induces tolerance in murine muscle as a result of poor APC transduction, T cell exhaustion, and minimal MHCI upregulation on target cells. Mol. Ther., 22, 28-41.
62. Klein, C.J., Coovert, D.D., Bulman, D.E., Ray, P.N., Mendell, J.R. and Burghes, A.H. (1992) Somatic reversion/suppression in Duchenne muscular dystrophy (DMD): evidence supporting a frame-restoring mechanism in rare dystrophin-positive fibers. Am. J. Hum. Genet., 50, 950-959.
63. Winnard, A.V., Mendell, J.R., Prior, T.W., Florence, J. and Burghes, A.H. (1995) Frameshift deletions of exons 3-7 and revertant fibers in Duchenne muscular dystrophy: mechanisms of dystrophin production. Am. J. Hum. Genet., 56, 158-166.
64. Kissel, J.T., Burrow, K.L., Rammohan, K.W. and Mendell, J.R. (1991) Mononuclear cell analysis of muscle biopsies in prednisone-treated and untreated Duchenne muscular dystrophy. CIDD Study Group. Neurology, 41, 667-672.
65. Appleyard, S.T., Dunn, M.J., Dubowitz, V. and Rose, M.L. (1985) Increased expression of HLA ABC class I antigens by muscle fibres in Duchenne muscular dystrophy, inflammatory myopathy, and other neuromuscular disorders. Lancet, 325,1, 361-363.
66. Karpati, G., Pouliot, Y. and Carpenter, S. (1988) Expression of immunoreactive major histocompatibility complex products in human skeletal muscles. Ann. Neurol., 23, 64-72.
67. Ronchetti, A., Rovere, P., Iezzi, G., Galati, G., Heltai, S., Protti, M.P., Garancini, M.P., Manfredi, A.A., Rugarli, C. and Bellone, M. (1999) Immunogenicity of apoptotic cells in vivo: role of antigen load, antigen-presenting cells, and cytokines. J. Immunol., 163, 130-136.
68. Bellone, M., Iezzi, G., Rovere, P., Galati, G., Ronchetti, A., Protti, M.P., Davoust, J., Rugarli, C. and Manfredi, A.A. (1997) Processing of engulfed apoptotic bodies yields T cell epitopes. J. Immunol, 159, 5391-5399.
69. Liao, N.S., Bix, M., Zijlstra, M., Jaenisch, R. and Raulet, D. (1991) MHC class I deficiency: susceptibility to natural killer (NK) cells and impaired NK activity. Science, 253, 199-202.
70. Solana, R., Serrano, R. and Pena, J. (1991) MHC antigens in NK cell recognition and lysis. Immunol. Today, 12, 95.
71. Pena, J. and Solana, R. (1992) Histocompatibility antigens and natural killer susceptibility. Immunol. Res., 11, 133-140.
72. Stern-Ginossar, N., Elefant, N., Zimmermann, A., Wolf, D.G., Saleh, N., Biton, M., Horwitz, E., Prokocimer, Z., Prichard, M., Hahn, G. et al. (2007) Host immune system gene targeting by a viral miRNA. Science, 317, 376-381.
73. Nachmani, D., Lankry, D., Wolf, D.G. and Mandelboim, O. The human cytomegalovirus microRNA miR-UL112 acts synergistically with a cellular microRNA to escape immune elimination. Nat. Immunol., 11, 806-813.
74. Neumann, L., Kraas, W., Uebel, S., Jung, G. and Tampe, R. (1997) The active domain of the herpes simplex virus protein ICP47: a potent inhibitor of the transporter associated with antigen processing. J. Mol. Biol., 272, 484-492.
75. Dugan, G.E. and Hewitt, E.W. (2008) Structural and Functional Dissection of the Human Cytomegalovirus Immune Evasion Protein US6. J. Virol., 82, 3271-3282.
76. Manno, C.S., Pierce, G.F., Arruda, V.R., Glader, B., Ragni, M., Rasko, J.J., Ozelo, M.C., Hoots, K., Blatt, P., Konkle, B. 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.
77. Nathwani, A.C., Tuddenham, E.G., Rangarajan, S., Rosales, C., McIntosh, J., Linch, D.C., Chowdary, P., Riddell, A., Pie, A.J., Harrington, C. et al. (2011) Adenovirus-associated virus vector-mediated gene transfer in hemophilia B. N. Engl. J. Med., 365, 2357-2365.
78. Nathwani, A.C., Reiss, U.M., Tuddenham, E.G., Rosales, C., Chowdary, P., McIntosh, J., Della Peruta, M., Lheriteau, E., Patel, N., Raj, D. et al. (2014) Long-term safety and efficacy of factor IX gene therapy in hemophilia B. N. Engl. J. Med., 371, 1994-2004.
79. Li, C., He, Y., Nicolson, S., Hirsch, M., Weinberg, M.S., Zhang, P., Kafri, T. and Samulski, R.J. (2013) Adeno-associated virus capsid antigen presentation is dependent on endosomal escape. J. Clin. Invest., 123, 1390-1401.
80. Mingozzi, F., Liu, Y.L., Dobrzynski, E., Kaufhold, A., Liu, J.H., Wang, Y., Arruda, V.R., High, K.A. and Herzog, R.W. (2003) Induction of immune tolerance to coagulation factor IX antigen by in vivo hepatic gene transfer. J. Clin. Invest., 111, 1347-1356.
81. Mingozzi, F., Hasbrouck, N.C., Basner-Tschakarjan, E., Edmonson, S.A., Hui, D.J., Sabatino, D.E., Zhou, S., Wright, J.F., Jiang, H., Pierce, G.F. et al. (2007) Modulation of tolerance to the transgene product in a nonhuman primate model of AAV-mediated gene transfer to liver. Blood, 110, 2334-2341.
82. Mingozzi, F. and High, K.A. (2017) Overcoming the host immune response to adeno-associated virus gene delivery vectors: the race between clearance, tolerance, neutralization, and escape. Ann. Rev. Virol., 4, 511-534.
83. Cao, O., Dobrzynski, E., Wang, L., Nayak, S., Mingle, B., Terhorst, C. and Herzog, R.W. (2007) Induction and role of regulatory CD4+CD25+ T cells in tolerance to the transgene product following hepatic in vivo gene transfer. Blood, 110, 1132-1140.
84. Mueller, C., Chulay, J.D., Trapnell, B.C., Humphries, M., Carey, B., Sandhaus, R.A., McElvaney, N.G., Messina, L., Tang, Q., Rouhani, F.N. et al. (2013) Human Treg responses allow sustained recombinant adeno-associated virus-mediated transgene expression. J. Clin. Invest., 123, 5310-5318.
85. Ferreira, V., Twisk, J., Kwikkers, K., Aronica, E., Brisson, D., Methot, J., Petry, H. and Gaudet, D. (2014) Immune responses to intramuscular administration of alipogene tiparvovec (AAV1-LPL(S447X)) in a phase II clinical trial of lipoprotein lipase deficiency gene therapy. Hum. Gene. Ther., 25, 180-188.
86. Xiao, X., Li, J. and Samulski, R.J. (1998) Production of high-titer recombinant adeno-associated virus vectors in the absence of helper adenovirus. J. Virol., 72, 2224-2232.
87. Halenius, A., Momburg, F., Reinhard, H., Bauer, D., Lobigs, M. and Hengel, H. (2006) Physical and functional interactions of the cytomegalovirus US6 glycoprotein with the transporter associated with antigen processing. J. Biol. Chem., 281, 5383-5390.
88. Qiao, J., Wang, H., Kottke, T., Diaz, R.M., Willmon, C., Hudacek, A., Thompson, J., Parato, K., Bell, J., Naik, J. et al. (2008) Loading of oncolytic vesicular stomatitis virus onto antigen-specific T cells enhances the efficacy of adoptive T-cell therapy of tumors. Gene. Ther., 15, 604-616.
89. Li, C., Goudy, K., Hirsch, M., Asokan, A., Fan, Y., Alexander, J., Sun, J., Monahan, P., Seiber, D., Sidney, J. et al. (2009) Cellular immune response to cryptic epitopes during therapeutic gene transfer. Proc. Natl. Acad. Sci. U S A, 106, 10770-10774.
90. Li, C., Hirsch, M., DiPrimio, N., Asokan, A., Goudy, K., Tisch, R. and Samulski, R.J. (2009) Cytotoxic-T-lymphocyte-mediated elimination of target cells transduced with engineered adeno-associated virus type 2 vector in vivo. J. Virol., 83, 6817-6824.