Virus infection recognition and early innate responses to non-enveloped viral vectors

Viruses

Volumn 2, Issue 1, 2010, Pages 244-261

  Shayakhmetov, Dmitry M ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

Inflammation; Innate immunity; Virus vectors

Indexed keywords

ADENOVIRUS VECTOR; CRYOPYRIN; DOUBLE STRANDED DNA; GAMMA INTERFERON INDUCIBLE PROTEIN 10; I KAPPA B KINASE BETA; INTERFERON REGULATORY FACTOR 3; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 1; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 4; INTERLEUKIN 24; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MACROPHAGE INFLAMMATORY PROTEIN 2; MITOGEN ACTIVATED PROTEIN KINASE 6; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN PROTEIN; PARVOVIRUS VECTOR; RANTES; RETINOIC ACID INDUCIBLE PROTEIN I; RETINOIC ACID RECEPTOR; SINGLE STRANDED RNA; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 9;

ADAPTIVE IMMUNITY; AMINO TERMINAL SEQUENCE; CARBOXY TERMINAL SEQUENCE; COXSACKIE VIRUS; CPG ISLAND; CYSTIC FIBROSIS; CYTOKINE PRODUCTION; DENDRITIC CELL; DIMERIZATION; DISSEMINATED INTRAVASCULAR CLOTTING; GENE TRANSLOCATION; HUMAN; INNATE IMMUNITY; LEUKOCYTE; MOLECULAR DYNAMICS; NEOPLASM; NEUTROPHIL CHEMOTAXIS; NONHUMAN; OLIGOMERIZATION; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; PROTEIN SYNTHESIS; REVIEW; SAFETY; SIGNAL TRANSDUCTION; VACCINATION; VESICULAR STOMATITIS VIRUS; VIRAL GENE THERAPY; VIRUS INFECTION;

ADENO-ASSOCIATED VIRUS; ADENOVIRIDAE;

EID: 79952077137     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v2010244     Document Type: Review

References (105)

1. Brunetti-Pierri, N.; Palmer, D.J.; Beaudet, A.L.; Carey, K.D.; Finegold, M.; Ng, P. Acute toxicity after high-dose systemic injection of helper-dependent adenoviral vectors into nonhuman primates. Hum. Gene Ther. 2004, 15, 35-46.
2. Raper, S.E.; Chirmule, N.; Lee, F.S.; Wivel, N.A.; Bagg, A.; Gao, G.P.; Wilson, J.M.; Batshaw, M.L. Fatal systemic inflammatory response syndrome in a ornithine transcarbamylase deficient patient following adenoviral gene transfer. Mol. Genet. Metab. 2003, 80, 148-158.
3. Raper, S.E.; Yudkoff, M.; Chirmule, N.; Gao, G.P.; Nunes, F.; Haskal, Z.J.; Furth, E.E.; Propert, K.J.; Robinson, M.B.; Magosin, S.; Simoes, H.; Speicher, L.; Hughes, J.; Tazelaar, J.; Wivel, N.A.; Wilson, J.M.; Batshaw, M.L. A pilot study of in vivo liver-directed gene transfer with an adenoviral vector in partial ornithine transcarbamylase deficiency. Hum. Gene Ther. 2002, 13, 163-175.
4. Richman, D.D.; Whitley, R.; Hayden, F.G. Clinical Virology, 2nd ed.; ASM Press: Washington, D.C., USA, 2002.
5. Takeuchi, O.; Akira, S. Innate immunity to virus infection. Immunol. Rev. 2009, 227, 75-86.
6. Takeda, K.; Akira, S. Toll-like receptors in innate immunity. Int. Immunol. 2005, 17, 1-14.
7. Alexopoulou, L.; Holt, A.C.; Medzhitov, R.; Flavell, R.A. Recognition of double-stranded RNA and activation of NF-kappa B by Toll-like receptor 3. Nature 2001, 413, 732-738.
8. Diebold, S.S.; Kaisho, T.; Hemmi, H.; Akira, S.; Reis e Sousa, C. Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 2004, 303, 1529-1531.
9. Heil, F.; Hemmi, H.; Hochrein, H.; Ampenberger, F.; Kirschning, C.; Akira, S.; Lipford, G.; Wagner, H.; Bauer, S. Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science 2004, 303, 1526-1529.
10. Lund, J.M.; Alexopoulou, L.; Sato, A.; Karow, M.; Adams, N.C.; Gale, N.W.; Iwasaki, A.; Flavell, R.A. Recognition of single-stranded RNA viruses by Toll-like receptor 7. Proc. Natl. Acad. Sci. USA 2004, 101, 5598-5603.
11. Hemmi, H.; Takeuchi, O.; Kawai, T.; Kaisho, T.; Sato, S.; Sanjo, H.; Matsumoto, M.; Hoshino, K.; Wagner, H.; Takeda, K.; Akira, S. A Toll-like receptor recognizes bacterial DNA. Nature 2000, 408, 740-745.
12. Colonna, M.; Trinchieri, G.; Liu, Y.J. Plasmacytoid dendritic cells in immunity. Nat. Immunol. 2004, 5, 1219-1226.
13. Kawai, T.; Akira, S. TLR signaling. Semin. Immunol. 2007, 19, 24-32.
14. Hoebe, K.; Du, X.; Georgel, P.; Janssen, E.; Tabeta, K.; Kim, S.O.; Goode, J.; Lin, P.; Mann, N.; Mudd, S.; Crozat, K.; Sovath, S.; Han, J.; Beutler, B. Identification of Lps2 as a key transducer of MyD88-independent TIR signalling. Nature 2003, 424, 743-748.
15. Oshiumi, H.; Matsumoto, M.; Funami, K.; Akazawa, T.; Seya, T. TICAM-1, an adaptor molecule that participates in Toll-like receptor 3-mediated interferon-beta induction. Nat. Immunol. 2003, 4, 161-167.
16. Yamamoto, M.; Sato, S.; Mori, K.; Hoshino, K.; Takeuchi, O.; Takeda, K.; Akira, S. Cutting edge: a novel Toll/IL-1 receptor domain-containing adapter that preferentially activates the IFN-beta promoter in the Toll-like receptor signaling. J. Immunol. 2002, 169, 6668-6672.
17. Yamamoto, M.; Sato, S.; Hemmi, H.; Hoshino, K.; Kaisho, T.; Sanjo, H.; Takeuchi, O.; Sugiyama, M.; Okabe, M.; Takeda, K.; Akira, S. Role of adaptor TRIF in the MyD88-independent toll-like receptor signaling pathway. Science 2003, 301, 640-643.
18. Deng, L.; Wang, C.; Spencer, E.; Yang, L.; Braun, A.; You, J.; Slaughter, C.; Pickart, C.; Chen, Z.J. Activation of the IkappaB kinase complex by TRAF6 requires a dimeric ubiquitin-conjugating enzyme complex and a unique polyubiquitin chain. Cell 2000, 103, 351-361.
19. Sharma, S.; tenOever, B.R.; Grandvaux, N.; Zhou, G.P.; Lin, R.; Hiscott, J. Triggering the interferon antiviral response through an IKK-related pathway. Science 2003, 300, 1148-1151.
20. Fitzgerald, K.A.; McWhirter, S.M.; Faia, K.L.; Rowe, D.C.; Latz, E.; Golenbock, D.T.; Coyle, A.J.; Liao, S.M.; Maniatis, T. IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat. Immunol. 2003, 4, 491-496.
21. Tabeta, K.; Georgel, P.; Janssen, E.; Du, X.; Hoebe, K.; Crozat, K.; Mudd, S.; Shamel, L.; Sovath, S.; Goode, J.; Alexopoulou, L.; Flavell, R. A.; Beutler, B. Toll-like receptors 9 and 3 as essential components of innate immune defense against mouse cytomegalovirus infection. P. Natl. Acad. Sci. USA 2004, 101, 3516-3521.
22. Takeuchi, O.; Takeda, K.; Hoshino, K.; Adachi, O.; Ogawa, T.; Akira, S. Cellular responses to bacterial cell wall components are mediated through MyD88-dependent signaling cascades. Int. Immunol. 2000, 12, 113-117.
23. Honda, K.; Yanai, H.; Mizutani, T.; Negishi, H.; Shimada, N.; Suzuki, N.; Ohba, Y.; Takaoka, A.; Yeh, W.C.; Taniguchi, T. Role of a transductional-transcriptional processor complex involving MyD88 and IRF-7 in Toll-like receptor signaling. Proc. Natl. Acad. Sci. USA 2004, 101, 15416-15421.
24. Kawai, T.; Sato, S.; Ishii, K.J.; Coban, C.; Hemmi, H.; Yamamoto, M.; Terai, K.; Matsuda, M.; Inoue, J.; Uematsu, S.; Takeuchi, O.; Akira, S. Interferon-alpha induction through Toll-like receptors involves a direct interaction of IRF7 with MyD88 and TRAF6. Nat. Immunol. 2004, 5, 1061-1068.
25. Lee, H.K.; Lund, J.M.; Ramanathan, B.; Mizushima, N.; Iwasaki, A. Autophagy-dependent viral recognition by plasmacytoid dendritic cells. Science 2007, 315, 1398-1401.
26. Zhu, J.G.; Huang, X.P.; Yang, Y.P. Innate immune response to adenoviral vectors is mediated by both Toll-like receptor-dependent and -independent pathways. J. Virol. 2007, 81, 3170-3180.
27. Kang, D.C.; Gopalkrishnan, R.V.; Wu, Q.; Jankowsky, E.; Pyle, A.M.; Fisher, P.B. mda-5: An interferon-inducible putative RNA helicase with double-stranded RNA-dependent ATPase activity and melanoma growth-suppressive properties. Proc. Natl. Acad. Sci. USA 2002, 99, 637-642.
28. Yoneyama, M.; Kikuchi, M.; Natsukawa, T.; Shinobu, N.; Imaizumi, T.; Miyagishi, M.; Taira, K.; Akira, S.; Fujita, T. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 2004, 5, 730-737.
29. Loo, Y.M.; Fornek, J.; Crochet, N.; Bajwa, G.; Perwitasari, O.; Martinez-Sobrido, L.; Akira, S.; Gill, M.A.; Garcia-Sastre, A.; Katze, M.G.; Gale, M., Jr. Distinct RIG-I and MDA5 signaling by RNA viruses in innate immunity. J. Virol. 2008, 82, 335-345.
30. Yoneyama, M.; Kikuchi, M.; Matsumoto, K.; Imaizumi, T.; Miyagishi, M.; Taira, K.; Foy, E.; Loo, Y.M.; Gale, M., Jr.; Akira, S.; Yonehara, S.; Kato, A.; Fujita, T. Shared and unique functions of the DExD/H-box helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity. J. Immunol. 2005, 175, 2851-2858.
31. Kato, H.; Takeuchi, O.; Mikamo-Satoh, E.; Hirai, R.; Kawai, T.; Matsushita, K.; Hiiragi, A.; Dermody, T.S.; Fujita, T.; Akira, S. Length-dependent recognition of double-stranded ribonucleic acids by retinoic acid-inducible gene-I and melanoma differentiation-associated gene 5. J. Exp. Med. 2008, 205, 1601-1610.
32. Hornung, V.; Ellegast, J.; Kim, S.; Brzozka, K.; Jung, A.; Kato, H.; Poeck, H.; Akira, S.; Conzelmann, K.K.; Schlee, M.; Endres, S.; Hartmann, G. 5 '-triphosphate RNA is the ligand for RIG-I. Science 2006, 314, 994-997.
33. Pichlmair, A.; Schulz, O.; Tan, C.P.; Naslund, T.I.; Liljestrom, P.; Weber, F.; Sousa, C.R.E. RIG-I-mediated antiviral responses to single-stranded RNA bearing 5 '-phosphates. Science 2006, 314, 997-1001.
34. Schmidt, A.; Schwerd, T.; Hamm, W.; Hellmuth, J.C.; Cui, S.; Wenzel, M.; Hoffmann, F.S.; Michallet, M.C.; Besch, R.; Hopfner, K.P.; Endres, S.; Rothenfusser, S. 5'-triphosphate RNA requires base-paired structures to activate antiviral signaling via RIG-I. Proc. Natl. Acad. Sci. USA 2009, 106, 12067-12072.
35. Kawai, T.; Takahashi, K.; Sato, S.; Coban, C.; Kumar, H.; Kato, H.; Ishii, K.J.; Takeuchi, O.; Akira, S. IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat. Immunol. 2005, 6, 981-988.
36. Meylan, E.; Curran, J.; Hofmann, K.; Moradpour, D.; Binder, M.; Bartenschlager, R.; Tschopp, R. Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 2005, 437, 1167-1172.
37. Seth, R.B.; Sun, L.J.; Ea, C.K.; Chen, Z.J.J. Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappa B and IRF3. Cell 2005, 122, 669-682.
38. Xu, L.G.; Wang, Y.Y.; Han, K.J.; Li, L.Y.; Zhai, Z.H.; Shu, H.B. VISA is an adapter protein required for virus-triggered IFN-beta signaling. Mol. Cell 2005, 19, 727-740.
39. Michallet, M.C.; Meylan, E.; Ermolaeva, M.A.; Vazquez, J.; Rebsamen, M.; Curran, J.; Poeck, H.; Bscheider, M.; Hartmann, G.; Konig, M.; Kalinke, U.; Pasparakis, M.; Tschopp, J. TRADD protein is an essential component of the RIG-like helicase antiviral pathway. Immunity 2008, 28, 651-661.
40. Oganesyan, G.; Saha, S.K.; Guo, B.; He, J.Q.; Shahangian, A.; Zarnegar, B.; Perry, A.; Cheng, G. Critical role of TRAF3 in the Toll-like receptor-dependent and -independent antiviral response. Nature 2006, 439, 208-211.
41. Melchjorsen, J.; Jensen, S.B.; Malmgaard, L.; Rasmussen, S.B.; Weber, F.; Bowie, A.G.; Matikainen, S.; Paludan, S.R. Activation of innate defense against a paramyxovirus is mediated by RIG-I and TLR7 and TLR8 in a cell-type-specific manner. J. Virol. 2005, 79, 12944-12951.
42. Sumpter, R., Jr.; Loo, Y.M.; Foy, E.; Li, K.; Yoneyama, M.; Fujita, T.; Lemon, S.M.; Gale, M., Jr. Regulating intracellular antiviral defense and permissiveness to hepatitis C virus RNA replication through a cellular RNA helicase, RIG-I. J. Virol. 2005, 79, 2689-2699.
43. Kato, H.; Sato, S.; Yoneyama, M.; Yamamoto, M.; Uematsu, S.; Matsui, K.; Tsujimura, T.; Takeda, K.; Fujita, T.; Takeuchi, O.; Akira, S. Cell type-specific involvement of RIG-I in antiviral response. Immunity 2005, 23, 19-28.
44. Kato, H.; Takeuchi, O.; Sato, S.; Yoneyama, M.; Yamamoto, M.; Matsui, K.; Uematsu, S.; Jung, A.; Kawai, T.; Ishii, K.J.; Yamaguchi, O.; Otsu, K.; Tsujimura, T.; Koh, C.S.; Reis e Sousa, C.; Matsuura, Y.; Fujita, T.; Akira, S. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 2006, 441, 101-105.
45. Gitlin, L.; Barchet, W.; Gilfillan, S.; Cella, M.; Beutler, B.; Flavell, R.A.; Diamond, M.S.; Colonna, M. Essential role of mda-5 in type I IFN responses to polyriboinosinic:polyribocytidylic acid and encephalomyocarditis picornavirus. Proc. Natl. Acad. Sci. U S A 2006, 103, 8459-8464.
46. Ye, Z.; Ting, J.P. NLR, the nucleotide-binding domain leucine-rich repeat containing gene family. Curr. Opin. Immunol. 2008, 20, 3-9.
47. Ting, J.P.Y.; Willingham, S.B.; Bergstralh, D.T. NLRs at the intersection of cell death and immunity. Nat. Rev. Immunol. 2008, 8, 372-379.
48. Lich, J.D.; Ting, J.P. CATERPILLER (NLR) family members as positive and negative regulators of inflammatory responses. Proc. Am. Thorac. Soc. 2007, 4, 263-266.
49. Sutterwala, F.S.; Ogura, Y.; Flavell, R.A. The inflammasome in pathogen recognition and inflammation. J. Leukocyte Biol. 2007, 82, 259-264.
50. Lamkanfi, M.; Kanneganti, T.D.; Franchi, L.; Nunez, G. Caspase-1 inflammasomes in infection and inflammation. J. Leukoc. Biol. 2007, 82, 220-225.
51. Martinon, F.; Mayor, A.; Tschopp, J. The inflammasomes: guardians of the body. Annu. Rev. Immunol. 2009, 27, 229-265.
52. Muruve, D.A.; Petrilli, V.; Zaiss, A.K.; White, L.R.; Clark, S.A.; Ross, P.J.; Parks, R.J.; Tschopp, J. The inflammasome recognizes cytosolic microbial and host DNA and triggers an innate immune response. Nature 2008, 452, 103-107.
53. Allen, I.C.; Scull, M.A.; Moore, C.B.; Holl, E.K.; McElvania-TeKippe, E.; Taxman, D.J.; Guthrie, E.H.; Pickles, R.J.; Ting, J.P. The NLRP3 inflammasome mediates in vivo innate immunity to influenza A virus through recognition of viral RNA. Immunity 2009, 30, 556-565.
54. Thomas, P.G.; Dash, P.; Aldridge, J.R., Jr.; Ellebedy, A.H.; Reynolds, C.; Funk, A.J.; Martin, W.J.; Lamkanfi, M.; Webby, R.J.; Boyd, K.L.; Doherty, P.C.; Kanneganti, T.D. The intracellular sensor NLRP3 mediates key innate and healing responses to influenza A virus via the regulation of caspase-1. Immunity 2009, 30, 566-575.
55. Takaoka, A.; Wang, Z.; Choi, M.K.; Yanai, H.; Negishi, H.; Ban, T.; Lu, Y.; Miyagishi, M.; Kodama, T.; Honda, K.; Ohba, Y.; Taniguchi, T. DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature 2007, 448, 501-505.
56. Ishii, K.J.; Coban, C.; Kato, H.; Takahashi, K.; Torii, Y.; Takeshita, F.; Ludwig, H.; Sutter, G.; Suzuki, K.; Hemmi, H.; Sato, S.; Yamamoto, M.; Uematsu, S.; Kawai, T.; Takeuchi, O.; Akira, S. A Toll-like receptor-independent antiviral response induced by double-stranded B-form DNA. Nat. Immunol. 2006, 7, 40-48.
57. Roberts, T.L.; Idris, A.; Dunn, J.A.; Kelly, G.M.; Burnton, C.M.; Hodgson, S.; Hardy, L.L.; Garceau, V.; Sweet, M.J.; Ross, I.L.; Hume, D.A.; Stacey, K.J. HIN-200 proteins regulate caspase activation in response to foreign cytoplasmic DNA. Science 2009, 323, 1057-1060.
58. Hornung, V.; Ablasser, A.; Charrel-Dennis, M.; Bauernfeind, F.; Horvath, G.; Caffrey, D.R.; Latz, E.; Fitzgerald, K.A., AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature 2009, 458, 514-518.
59. Fernandes-Alnemri, T.; Yu, J.W.; Datta, P.; Wu, J.; Alnemri, E.S. AIM2 activates the inflammasome and cell death in response to cytoplasmic DNA. Nature 2009, 458, 509-513.
60. Burckstummer, T.; Baumann, C.; Bluml, S.; Dixit, E.; Durnberger, G.; Jahn, H.; Planyavsky, M.; Bilban, M.; Colinge, J.; Bennett, K.L.; Superti-Furga, G. An orthogonal proteomic-genomic screen identifies AIM2 as a cytoplasmic DNA sensor for the inflammasome. Nat. Immunol. 2009, 10, 266-272.
61. Schroder, K.; Muruve, D.A.; Tschopp, J. Innate immunity: cytoplasmic DNA sensing by the AIM2 inflammasome. Curr. Biol. 2009, 19, R262-265.
62. Chen, Z.; Benureau, Y.; Rijnbrand, R.; Yi, J.; Wang, T.; Warter, L.; Lanford, R.E.; Weinman, S.A.; Lemon, S.M.; Martin, A.; Li, K. GB virus B disrupts RIG-I signaling by NS3/4A-mediated cleavage of the adaptor protein MAVS. J. Virol. 2007, 81, 964-976.
63. Baril, M.; Racine, M.E.; Penin, F.; Lamarre, D. MAVS dimer is a crucial signaling component of innate immunity and the target of hepatitis C virus NS3/4A protease. J. Virol. 2009, 83, 1299-1311.
64. Hutchin, M.E.; Pickles, R.J.; Yarbrough, W.G. Efficiency of adenovirus-mediated gene transfer to oropharyngeal epithelial cells correlates with cellular differentiation and human coxsackie and adenovirus receptor expression. Hum. Gene Ther. 2000, 11, 2365-2375.
65. Kobinger, G.P., Feldmann, F., Schumer, G.P., Roy, S., Gao, G., Jones, S.M., Wilson, J.M. Simian adenoviral vector expressing Ebola glycoprotein variants for safe establishment of a strong protective immunity. Mol. Ther. 2003, 7, S310.
66. Tan Y.H.N., Lee J., Vintayen, E.; Crystal, R.G. Rapid protective immunity evoked against anthrax lethal toxin following a single intramuscular administration of an adenovirus-based vaccine coding for humanized protective antigen. Mol. Ther. 2003, 7, S311.
67. Morral, N.; O'Neal, W.K.; Rice, K.; Leland, M.M.; Piedra, P.A.; Aguilar-Cordova, E.; Carey, K.D.; Beaudet, A.L.; Langston, C. Lethal toxicity, severe endothelial injury, and a threshold effect with high doses of an adenoviral vector in baboons. Hum. Gene. Ther. 2002, 13, 143-154.
68. Lozier, J.N.; Csako, G.; Mondoro, T.H.; Krizek, D.M.; Metzger, M.E.; Costello, R.; Vostal, J.G.; Rick, M.E.; Donahue, R.E.; Morgan, R.A. Toxicity of a first-generation adenoviral vector in rhesus macaques. Hum. Gene Ther. 2002, 13, 113-124.
69. Alemany, R.; Suzuki, K.; Curiel, D.T. Blood clearance rates of adenovirus type 5 in mice. J. Gen. Virol. 2000, 81, 2605-2609.
70. Kirn, D. Clinical research results with dl1520 (Onyx-015), a replication-selective adenovirus for the treatment of cancer: what have we learned? Gene Ther. 2001, 8, 89-98.
71. Kirn, D.; Martuza, R.L.; Zwiebel, J. Replication-selective virotherapy for cancer: Biological principles, risk management and future directions. Nat. Med. 2001, 7, 781-787.
72. Tao, N.; Gao, G.P.; Parr, M.; Johnston, J.; Baradet, T.; Wilson, J.M.; Barsoum, J.; Fawell, S.E. Sequestration of adenoviral vector by Kupffer cells leads to a nonlinear dose response of transduction in liver. Mol. Ther. 2001, 3, 28-35.
73. Worgall, S.; Wolff, G.; Falck-Pedersen, E.; Crystal, R.G. Innate immune mechanisms dominate elimination of adenoviral vectors following in vivo administration. Hum. Gene Ther. 1997, 8, 37-44.
74. Wolff, G.; Worgall, S.; van Rooijen, N.; Song, W.R.; Harvey, B.G.; Crystal, R.G. Enhancement of in vivo adenovirus-mediated gene transfer and expression by prior depletion of tissue macrophages in the target organ. J. Virol. 1997, 71, 624-629.
75. Liu, Q.; Muruve, D.A. Molecular basis of the inflammatory response to adenovirus vectors. Gene Ther. 2003, 10, 935-940.
76. Lieber, A.; He, C.Y.; Meuse, L.; Schowalter, D.; Kirillova, I.; Winther, B.; Kay, M.A. The role of Kupffer cell activation and viral gene expression in early liver toxicity after infusion of recombinant adenovirus vectors. J. Virol. 1997, 71, 8798-8807.
77. Schnell, M.A.; Zhang, Y.; Tazelaar, J.; Gao, G.P.; Yu, Q.C.; Qian, R.; Chen, S.J.; Varnavski, A.N.; LeClair, C.; Raper, S.E.; Wilson, J.M. Activation of innate immunity in nonhuman primates following intraportal administration of adenoviral vectors. Mol. Ther. 2001, 3, 708-722.
78. Zhang, Y.; Chirmule, N.; Gao, G.P.; Qian, R.; Croyle, M.; Joshi, B.; Tazelaar, J.; Wilson, J.M. Acute cytokine response to systemic adenoviral vectors in mice is mediated by dendritic cells and macrophages. Mol. Ther. 2001, 3, 697-707.
79. Muruve, D.A.; Barnes, M.J.; Stillman, I.E.; Libermann, T.A. Adenoviral gene therapy leads to rapid induction of multiple chemokines and acute neutrophil-dependent hepatic injury in vivo. Hum. Gene Ther. 1999, 10, 965-976.
80. Borgland, S.L.; Bowen, G.P.; Wong, N.C.; Libermann, T.A.; Muruve, D.A. Adenovirus vector-induced expression of the C-X-C chemokine IP-10 is mediated through capsid-dependent activation of NF-kappaB. J. Virol. 2000, 74, 3941-3947.
81. Bowen, G.P.; Borgland, S.L.; Lam, M.; Libermann, T.A.; Wong, N.C.; Muruve, D.A. Adenovirus vector-induced inflammation: capsid-dependent induction of the C-C chemokine RANTES requires NF-kappa B. Hum. Gene Ther. 2002, 13, 367-379.
82. Bhat, N.R.; Fan, F. Adenovirus infection induces microglial activation: involvement of mitogen-activated protein kinase pathways. Brain Res. 2002, 948, 93-101.
83. Reid, T.; Galanis, E.; Abbruzzese, J.; Sze, D.; Andrews, J.; Romel, L.; Hatfield, M.; Rubin, J.; Kirn, D. Intra-arterial administration of a replication-selective adenovirus (dl1520) in patients with colorectal carcinoma metastatic to the liver: a phase I trial. Gene Ther. 2001, 8, 1618-1626.
84. Crystal, R.G.; Harvey, B.G.; Wisnivesky, J.P.; O'Donoghue, K.A.; Chu, K.W.; Maroni, J.; Muscat, J.C.; Pippo, A.L.; Wright, C.E.; Kaner, R.J.; Leopold, P.L.; Kessler, P.D.; Rasmussen, H.S.; Rosengart, T.K.; Hollmann, C. Analysis of risk factors for local delivery of low- and intermediate-dose adenovirus gene transfer vectors to individuals with a spectrum of comorbid conditions. Hum. Gene Ther. 2002, 13, 65-100.
85. Ben-Gary, H.; McKinney, R.L.; Rosengart, T.; Lesser, M.L.; Crystal, R.G. Systemic interleukin-6 responses following administration of adenovirus gene transfer vectors to humans by different routes. Mol. Ther. 2002, 6, 287-297.
86. Mickelson, C.A. Department of Health and Human Services National Institutes of Health Recombinant DNA Advisory Committee. Minutes of meeting March 8-10, 2000. Hum. Gene Ther. 2000, 11, 2159-2192.
87. McCoy, R.D.; Davidson, B.L.; Roessler, B.J.; Huffnagle, G.B.; Janich, S.L.; Laing, T.J.; Simon, R.H. Pulmonary inflammation induced by incomplete or inactivated adenoviral particles. Hum. Gene Ther. 1995, 6, 1553-1560.
88. Fejer, G.; Drechsel, L.; Liese, J.; Schleicher, U.; Ruzsics, Z.; Imelli, N.; Greber, U.F.; Keck, S.; Hildenbrand, B.; Krug, A.; Bogdan, C.; Freudenberg, M.A. Key Role of Splenic Myeloid DCs in the IFN-alpha beta Response to Adenoviruses In Vivo. Plos Pathog. 2008, 4, e1000208.
89. Nociari, M.; Ocheretina, O.; Schoggins, J.W.; Falck-Pedersen, E. Sensing infection by adenovirus: Toll-like receptor-independent viral DNA recognition signals activation of the interferon regulatory factor 3 master regulator. J. Virol. 2007, 81, 4145-4157.
90. Zhu, J.G.; Huang, X.P.; Yang, Y.P. Type IIFN signaling on both B and CD4 T cells is required for protective antibody response to adenovirus. J. Immunol. 2007, 178, 3505-3510.
91. Hartman, Z.C.; Kiang, A.; Everett, R.S.; Serra, D.; Yang, X.Y.; Clay, T.M.; Amalfitano, A. Adenovirus infection triggers a rapid, MyD88-regulated transcriptome response critical to acute-phase and adaptive immune responses in vivo. J. Virol. 2007, 81, 1796-1812.
92. Hartman, Z.C.; Black, E.P.; Amalfitano, A. Adenoviral infection induces a multi-faceted innate cellular immune response that is mediated by the toll-like receptor pathway in A549 cells. Virology 2007, 358, 357-372.
93. Iacobelli-Martinez, M.; Nemerow, G.R. Preferential activation of toll-like receptor nine by CD46-utilizing adenoviruses. J. Virol. 2007, 81, 1305-1312.
94. Basner-Tschakarjan, E.; Gaffal, E.; O'Keeffe, M.; Tormo, D.; Limmer, A.; Wagner, H.; Hochrein, H.; Tuting, T. Adenovirus efficiently transduces plasmacytoid dendritic cells resulting in TLR9-dependent maturation and IFN-alpha production. J. Gene Med. 2006, 8, 1300-1306.
95. Shayakhmetov, D.M.; Li, Z.Y.; Ternovoi, V.; Gaggar, A.; Gharwan, H.; Lieber, A. The interaction between the fiber knob domain and the cellular attachment receptor determines the intracellular trafficking route of adenoviruses. J. Virol. 2003, 77, 3712-3723.
96. Cerullo, V.; Seiler, M.P.; Mane, V.; Brunetti-Pierri, N.; Clarke, C.; Bertin, T.K.; Rodgers, J.R.; Lee, B. Toll-like receptor 9 triggers an innate immune response to helper-dependent adenoviral vectors. Mol. Ther. 2007, 15, 378-385.
97. Di Paolo, N.C.; Miao, E.A.; Iwakura, Y.; Murali-Krishna, K.; Aderem, A.; Flavell, R.A.; Papayannopoulou, T.; Shayakhmetov, D.M. Virus binding to a plasma membrane receptor triggers interleukin-1 alpha-mediated proinflammatory macrophage response in vivo. Immunity 2009, 31, 110-121.
98. Wickham, T.J.; Mathias, P.; Cheresh, D.A.; Nemerow, G.R. Integrins alpha v beta 3 and alpha v beta 5 promote adenovirus internalization but not virus attachment. Cell 1993, 73, 309-319.
99. Greber, U.F.; Willetts, M.; Webster, P.; Helenius, A. Stepwise dismantling of adenovirus 2 during entry into cells. Cell 1993, 75, 477-486.
100. Chen, C.J.; Kono, H.; Golenbock, D.; Reed, G.; Akira, S.; Rock, K.L. Identification of a key pathway required for the sterile inflammatory response triggered by dying cells. Nat. Med. 2007, 13, 851-856.
101. McCaffrey, A.P.; Fawcett, P.; Nakai, H.; McCaffrey, R.L.; Ehrhardt, A.; Pham, T.T.; Pandey, K.; Xu, H.; Feuss, S.; Storm, T.A.; Kay, M.A. The host response to adenovirus, helper-dependent adenovirus, and adeno-associated virus in mouse liver. Mol. Ther. 2008, 16, 931-941.
102. Hasbrouck, N.C.; High, K.A. AAV-mediated gene transfer for the treatment of hemophilia B: problems and prospects. Gene Ther. 2008, 15, 870-875.
103. Mingozzi, F.; High, K.A. Immune responses to AAV in clinical trials. Curr. Gene Ther. 2007, 7, 316-324.
104. Zaiss, A.K.; Liu, Q.; Bowen, G.P.; Wong, N.C.; Bartlett, J.S.; Muruve, D.A. Differential activation of innate immune responses by adenovirus and adeno-associated virus vectors. J. Virol. 2002, 76, 4580-4590.
105. Zhu, J.; Huang, X.; Yang, Y. The TLR9-MyD88 pathway is critical for adaptive immune responses to adeno-associated virus gene therapy vectors in mice. J. Clin. Invest. 2009, 119, 2388-2398.