MyD88-dependent silencing of transgene expression during the innate and adaptive immune response to helper-dependent adenovirus

Human Gene Therapy

Volumn 21, Issue 3, 2010, Pages 325-336

  Suzuki, Masataka ^a   Cerullo, Vincenzo ^a,b   Bertin, Terry K ^a   Cela, Racel ^a   Clarke, Christian ^a   Guenther, Margaretha ^a   Brunetti Pierri, Nicola ^a   Lee, Brendan ^a,c  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF HELSINKI   (Finland)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; CYTOKINE; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR 2;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; EMBRYO; FIBROBLAST; GENE EXPRESSION; GENE SILENCING; GENETIC TRANSCRIPTION; INNATE IMMUNITY; MALE; MOUSE; NONHUMAN; TRANSGENE; VIRAL GENE DELIVERY SYSTEM; WILD TYPE;

ADAPTIVE IMMUNITY; ADENOVIRIDAE; ANIMALS; ANTIGEN-PRESENTING CELLS; BLOTTING, WESTERN; BONE MARROW; CELLS, CULTURED; CHROMATIN IMMUNOPRECIPITATION; CYTOKINES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FIBROBLASTS; FLOW CYTOMETRY; GENE SILENCING; GENETIC VECTORS; HELPER VIRUSES; IMMUNITY, INNATE; INTERFERON-GAMMA; LIVER; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYELOID DIFFERENTIATION FACTOR 88; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SPLEEN; TH1 CELLS; TOLL-LIKE RECEPTOR 2; TRANSGENES;

ADENOVIRIDAE; ANIMALIA; MUS;

EID: 77949770727     PISSN: 10430342     EISSN: None     Source Type: Journal    
DOI: 10.1089/hum.2009.155     Document Type: Article

References (45)

1. Adachi, O., Kawai, T., Takeda, K., Matsumoto, M., Tsutsui, H., Sakagami, M., Nakanishi, K., and Akira, S. (1998). Targeted disruption of the MyD88 gene results in loss of IL-1-and IL-18-mediated function. Immunity 9, 143-150.
2. Akira, S., Uematsu, S., and Takeuchi, O. (2006). Pathogen recognition and innate immunity. Cell 124, 783-801.
3. Appledorn, D.M., Patial, S., McBride, A., Godbehere, S., Van Rooijen, N., Parameswaran, N., and Amalfitano, A. (2008). Adenovirus vector-induced innate inflammatory mediators, MAPK signaling, as well as adaptive immune responses are dependent upon both TLR2 and TLR9 in vivo. J. Immunol. 181, 2134-2144.
4. Barcia, C., Jimenez-Dalmaroni, M., Kroeger, K.M., Puntel, M., Rapaport, A.J., Larocque, D., King, G.D., Johnson, S.A., Liu, C., Xiong, W., Candolfi, M., Mondkar, S., Ng, P., Palmer, D., Castro, M.G., and Lowenstein, P.R. (2007). One-year expression from high-capacity adenoviral vectors in the brains of animals with pre-existing anti-adenoviral immunity: Clinical implications. Mol. Ther. 15, 2154-2163.
5. Basner-Tschakarjan, E., Gaffal, E., O'Keeffe, M., Tormo, D., Limmer, A., Wagner, H., Hochrein, H., and Tuting, T. (2006). Adenovirus efficiently transduces plasmacytoid dendritic cells resulting in TLR9-dependent maturation and IFN-a production. J. Gene Med. 8, 1300-1306.
6. Bird, A.P., and Wolffe, A.P. (1999). Methylation-induced repression: Belts, braces, and chromatin. Cell 99, 451-454.
7. Bonnert, T.P., Garka, K.E., Parnet, P., Sonoda, G., Testa, J.R., and Sims, J.E. (1997). The cloning and characterization of human MyD88: A member of an IL-1 receptor related family. FEBS Lett. 402, 81-84.
8. Brunetti-Pierri, N., Palmer, D.J., Beaudet, A.L., Carey, K.D., Finegold, M., and Ng, P. (2004). Acute toxicity after high-dose systemic injection of helper-dependent adenoviral vectors into nonhuman primates. Hum. Gene Ther. 15, 35-46.
9. Brunetti-Pierri, N., Nichols, T.C., McCorquodale, S., Merricks, E., Palmer, D.J., Beaudet, A.L., and Ng, P. (2005). Sustained phenotypic correction of canine hemophilia B after systemic administration of helper-dependent adenoviral vector. Hum. Gene Ther. 16, 811-820.
10. Brunetti-Pierri, N., Ng, T., Iannitti, D.A., Palmer, D.J., Beaudet, A.L., Finegold, M.J., Carey, K.D., Cioffi, W.G., and Ng, P. (2006). Improved hepatic transduction, reduced systemic vector dissemination, and long-term transgene expression by delivering helper-dependent adenoviral vectors into the surgically isolated liver of nonhuman primates. Hum. Gene Ther. 17, 391-404.
11. Brunetti-Pierri, N., Clarke, C., Mane, V., Palmer, D.J., Lanpher, B., Sun, Q., O'Brien, W., and Lee, B. (2008). Phenotypic correction of ornithine transcarbamylase deficiency using low dose helper-dependent adenoviral vectors. J. Gene Med. 10, 890-896.
12. Brunetti-Pierri, N., Stapleton, G.E., Law, M., Breinholt, J., Palmer, D.J., Zuo, Y., Grove, N.C., Finegold, M.J., Rice, K., Beaudet, A.L., Mullins, C.E., and Ng, P. (2009). Efficient, long-term hepatic gene transfer using clinically relevant HDAd doses by balloon occlusion catheter delivery in nonhuman primates. Mol. Ther. 17, 327-333.
13. Burckstummer, T., Baumann, C., Bluml, S., Dixit, E., Durnberger, G., Jahn, H., Planyavsky, M., Bilban, M., Colinge, J., Bennett, K.L., and Superti-Furga, G. (2009). An orthogonal proteomic-genomic screen identifies AIM2 as a cytoplasmic DNA sensor for the inflammasome. Nat. Immunol. 10, 266-272.
14. Cerullo, V., Seiler, M.P., Mane, V., Brunetti-Pierri, N., Clarke, C., Bertin, T.K., Rodgers, J.R., and Lee, B. (2007a). Toll-like receptor 9 triggers an innate immune response to helper-dependent adenoviral vectors. Mol. Ther. 15, 378-385.
15. Cerullo, V., Seiler, M.P., Mane, V., Cela, R., Clarke, C., Kaufman, R.J., Pipe, S.W., and Lee, B. (2007b). Correction of murine hemophilia A and immunological differences of factor VIII variants delivered by helper-dependent adenoviral vectors. Mol. Ther. 15, 2080-2087.
16. Chen, Z.Y., Riu, E., He, C.Y., Xu, H., and Kay, M.A. (2008). Silencing of episomal transgene expression in liver by plasmid bacterial backbone DNA is independent of CpG methylation. Mol. Ther. 16, 548-556.
17. Garcia-Sastre, A., and Biron, C.A. (2006). Type 1 interferons and the virus-host relationship: A lesson in detente. Science 312, 879-882.
18. Gau, C.L., Rosenblatt, R.A., Cerullo, V., Lay, F.D., Dow, A.C., Livesay, J., Brunetti-Pierri, N., Lee, B., Cederbaum, S.D., Grody, W.W., and Lipshutz, G.S. (2009). Short-term correction of arginase deficiency in a neonatal murine model with a helper-dependent adenoviral vector. Mol. Ther. 17, 1155-1163.
19. Guo, B., Chang, E.Y., and Cheng, G. (2008). The type I IFN induction pathway constrains Th17-mediated autoimmune inflammation in mice. J. Clin. Invest. 118, 1680-1690.
20. Hartman, Z.C., Kiang, A., Everett, R.S., Serra, D., Yang, X.Y., Clay, T.M., and Amalfitano, A. (2007). Adenovirus infection triggers a rapid, MyD88-regulated transcriptome response critical to acute-phase and adaptive immune responses in vivo. J. Virol. 81, 1796-1812.
21. Hensley, S.E., and Amalfitano, A. (2007). Toll-like receptors impact on safety and efficacy of gene transfer vectors. Mol. Ther. 15, 1417-1422
22. Hensley, S.E., Cun, A.S., Giles-Davis, W., Li, Y., Xiang, Z., Lasaro, M.O., Williams, B.R., Silverman, R.H., and Ertl, H.C. (2007). Type I interferon inhibits antibody responses induced by a chimpanzee adenovirus vector. Mol. Ther. 15, 393-403.
23. Iacobelli-Martinez, M., and Nemerow, G.R. (2007). Preferential activation of Toll-like receptor nine by CD46-utilizing adeno-viruses. J. Virol. 81, 1305-1312.
24. Koizumi, N., Yamaguchi, T., Kawabata, K., Sakurai, F., Sasaki, T., Watanabe, Y., Hayakawa, T., and Mizuguchi, H. (2007). Fiber-modified adenovirus vectors decrease liver toxicity through reduced IL-6 production. J. Immunol. 178, 1767-1773.
25. Liu, S., Salyapongse, A.N., Geller, D.A., Vodovotz, Y., and Bil-liar, T.R. (2000). Hepatocyte Toll-like receptor 2 expression in vivo and in vitro: Role of cytokines in induction of rat TLR2 gene expression by lipopolysaccharide. Shock 14, 361-365.
26. Manickan, E., Smith, J.S., Tian, J., Eggerman, T.L., Lozier, J.N., Muller, J., and Byrnes, A.P. (2006). Rapid Kupffer cell death after intravenous injection of adenovirus vectors. Mol. Ther. 13, 108-117.
27. 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., Dake, M., Kaye, R., Razavi, M., Zajko, A., Zehnder, J., Rustagi, P.K., Nakai, H., Chew, A., Leonard, D., Wright, J.F., Lessard, R.R., Sommer, J.M., Tigges, M., Sabatino, D., Luk, A., Jiang, H., Mingozzi, F., Couto, L., Ertl, H.C., High, K.A., and Kay, M.A. (2006). Successful transduction of liver in hemophilia by AAV-Factor IX and limitations imposed by the host immune response. Nat. Med. 12, 342-347.
28. McCormack, W.M., Jr., Seiler, M.P., Bertin, T.K., Ubhayakar, K., Palmer, D.J., Ng, P., Nichols, T.C., and Lee, B. (2006). Helper-dependent adenoviral gene therapy mediates long-term correction of the clotting defect in the canine hemophilia A model. J. Thromb. Haemost. 4, 1218-1225.
29. Mian, A., McCormack, W.M., Jr., Mane, V., Kleppe, S., Ng, P., Finegold, M., O'Brien, W.E., Rodgers, J.R., Beaudet, A.L., and Lee, B. (2004). Long-term correction of ornithine transcarba-mylase deficiency by WPRE-mediated overexpression using a helper-dependent adenovirus. Mol. Ther. 10, 492-499.
30. Mian, A., Guenther, M., Finegold, M., Ng, P., Rodgers, J., and Lee, B. (2005). Toxicity and adaptive immune response to intracel-lular transgenes delivered by helper-dependent vs. first generation adenoviral vectors. Mol. Genet. Metab. 84, 278-288.
31. Morral, N., O'Neal, W.K., Rice, K., Leland, M.M., Piedra, P.A., Aguilar-Cordova, E., Carey, K.D., Beaudet, A.L., and Lang-ston, C. (2002). Lethal toxicity, severe endothelial injury, and a threshold effect with high doses of an adenoviral vector in baboons. Hum. Gene Ther. 13, 143-154.
32. Muruve, D.A. (2004). The innate immune response to adenovi-rus vectors. Hum. Gene Ther. 15, 1157-1166.
33. Muruve, D.A., Barnes, M.J., Stillman, I.E., and Libermann, T.A. (1999). Adenoviral gene therapy leads to rapid induction of multiple chemokines and acute neutrophil-dependent hepatic injury in vivo. Hum. Gene Ther. 10, 965-976.
34. Muruve, D.A., Cotter, M.J., Zaiss, A.K., White, L.R., Liu, Q., Chan, T., Clark, S.A., Ross, P.J., Meulenbroek, R.A., Mae-landsmo, G.M., and Parks, R.J. (2004). Helper-dependent ad-enovirus vectors elicit intact innate but attenuated adaptive host immune responses in vivo. J. Virol. 78, 5966-5972.
35. Niesner, U., Albrecht, I., Janke, M., Doebis, C., Loddenkemper, C., Lexberg, M.H., Eulenburg, K., Kreher, S., Koeck, J., Baumgrass, R., Bonhagen, K., Kamradt, T., Enghard, P., Humrich, J.Y., Rutz, S., Schulze-Topphoff, U., Aktas, O., Bartfeld, S., Rad-bruch, H., Hegazy, A.N., Löhning, M., Baumgart, D.C., Duch-mann, R., Rudwaleit, M., Häupl, T., Gitelman, I., Krenn, V., Gruen, J., Sieper, J., Zeitz, M., Wiedenmann, B., Zipp, F., Hamann, A., Janitz, M., Scheffold, A., Burmester, G.R., Chang, H.D., and Radbruch, A. (2008). Autoregulation of Th1-mediated inflammation by twist1. J. Exp. Med. 205, 1889-1901.
36. Nociari, M., Ocheretina, O., Schoggins, J.W., and Falck-Pedersen, E. (2007). Sensing infection by adenovirus: Toll-like receptor-independent viral DNA recognition signals activation of the interferon regulatory factor 3 master regulator. J. Virol. 81, 4145-4157.
37. Palmer, D., and Ng, P. (2003). Improved system for helper-dependent adenoviral vector production. Mol. Ther. 8, 846-852.
38. Parks, R.J., Chen, L., Anton, M., Sankar, U., Rudnicki, M.A., and Graham, F.L. (1996). A helper-dependent adenovirus vector system: Removal of helper virus by Cre-mediated excision of the viral packaging signal. Proc. Natl. Acad. Sci. U.S.A. 93, 13565-13570.
39. Sato, N., Takahashi, N., Suda, K., Nakamura, M., Yamaki, M., Ninomiya, T., Kobayashi, Y., Takada, H., Shibata, K., Yama-moto, M., Takeda, K., Akira, S., Noguchi, T., and Udagawa, N. (2004). MyD88 but not TRIF is essential for osteoclastogenesis induced by lipopolysaccharide, diacyl lipopeptide, and IL-1a. J. Exp. Med. 200, 601-611.
40. Suzuki, M., Chiocca, E.A., and Saeki, Y. (2007). Early STAT1 activation after systemic delivery of HSV amplicon vectors suppresses transcription of the vector-encoded transgene. Mol. Ther. 15, 2017-2026.
41. Suzuki, M., Kasai, K., Ohtsuki, A., Godlewski, J., Nowicki, M.O., Chiocca, E.A., and Saeki, Y. (2009). ICP0 inhibits the decrease of HSV amplicon-mediated transgene expression. Mol. Ther. 17, 707-715.
42. Toietta, G., Mane, V.P., Norona, W.S., Finegold, M.J., Ng, P., McDonagh, A.F., Beaudet, A.L., and Lee, B. (2005). Lifelong elimination of hyperbilirubinemia in the Gunn rat with a single injection of helper-dependent adenoviral vector. Proc. Natl. Acad. Sci. U.S.A. 102, 3930-3935.
43. Yamaguchi, T., Kawabata, K., Koizumi, N., Sakurai, F., Naka-shima, K., Sakurai, H., Sasaki, T., Okada, N., Yamanishi, K., and Mizuguchi, H. (2007). Role of MyD88 and TLR9 in the innate immune response elicited by serotype 5 adenoviral vectors. Hum. Gene Ther. 18, 753-762.
44. Zhang, Y., and Reinberg, D. (2001). Transcription regulation by histone methylation: Interplay between different covalent modifications of the core histone tails. Genes Dev. 15, 2343-2360.
45. Zhu, J., Huang, X., and Yang, Y. (2007). Innate immune response to adenoviral vectors is mediated by both Toll-like receptor-dependent and-independent pathways. J. Virol. 81, 3170-3180.