Dendritic cell maturation, but not CD8+ T cell induction, is dependent on type I IFN signaling during vaccination with adenovirus vectors

Journal of Immunology

Volumn 175, Issue 9, 2005, Pages 6032-6041

  Hensley, Scott E ^a,b   Giles Davis, Wynetta ^b   McCoy, Kimberly C ^b   Weninger, Wolfgang ^b   Ertl, Hildegund C J ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b WISTAR INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; CD8 ANTIGEN; EPIDERMAL GROWTH FACTOR RECEPTOR; GENE PRODUCT; INTERFERON; PHOSPHATIDYLINOSITOL 3 KINASE; T LYMPHOCYTE RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; ARTICLE; CELL MATURATION; CHIMPANZEE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; EMBRYO; HUMAN; HUMAN CELL; IMMUNE RESPONSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TRANSGENE; VACCINATION; VIRUS REPLICATION; VIRUS TRANSCRIPTION;

EID: 27144508046     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.175.9.6032     Document Type: Article

References (55)

1. Tatsis, N., and H. C. Ertl. 2004. Adenoviruses as vaccine vectors. Mol. Ther. 10: 616-629.
2. Gao, W., P. D. Robbins, and A. Gambotto. 2003. Human adenovirus type 35: nucleotide sequence and vector development. Gene Ther. 10: 1941-1949.
3. Vogels, R., D. Zuijdgeest, R. van Rijnsoever, E. Hartkoorn, I. Damen, M. P. de Bethune, S. Kostense, G. Penders, N. Helmus, W. Koudstaal, et al. 2003. Replication-deficient human adenovirus type 35 vectors for gene transfer and vaccination: efficient human cell infection and bypass of preexisting adenovirus immunity. J. Virol. 77: 8263-8271.
4. Holterman, L., R. Vogels, R. van der Vlugt, M. Sieuwerts, J. Grimbergen, J. Kaspers, E. Geelen, E. van der Helm, A. Lemckert, G. Gillissen, et al. 2004. Novel replication-incompetent vector derived from adenovirus type 11 (Ad11) for vaccination and gene therapy: low seroprevalence and non-cross-reactivity with Ad5. J. Virol. 78: 13207-13215.
5. Farina, S. F., G. P. Gao, Z. Q. Xiang, J. J. Rux, R. M. Burnett, M. R. Alvira, J. Marsh, H. C. Ertl, and J. M. Wilson. 2001. Replication-defective vector based on a chimpanzee adenovirus. J. Virol. 75: 11603-11613.
6. Roy, S., G. Gao, Y. Lu, X. Zhou, M. Lock, R. Calcedo, and J. M. Wilson. 2004. Characterization of a family of chimpanzee adenoviruses and development of molecular clones for gene transfer vectors. Hum. Gene Ther. 15: 519-530.
7. Fitzgerald, J. C., G. P. Gao, A. Reyes-Sandoval, G. N. Pavlakis, Z. Q. Xiang, A. P. Wlazlo, W. Giles-Davis, J. M. Wilson, and H. C. Ertl. 2003. A simian replication-defective adenoviral recombinant vaccine to HIV-1 gag. J. Immunol. 170: 1416-1422.
8. Reyes-Sandoval, A., J. C. Fitzgerald, R. Grant, S. Roy, Z. Q. Xiang, Y. Li, G. P. Gao, J. M. Wilson, and H. C. Ertl. 2004. Human immunodeficiency virus type 1-specific immune responses in primates upon sequential immunization with adenoviral vaccine carriers of human and simian serotypes. J. Virol. 78: 7392-7399.
9. Banchereau, J., and R. M. Steinman. 1998. Dendritic cells and the control of immunity. Nature 392: 245-252.
10. Di Nicola, M., S. Siena, M. Bregni, P. Longoni, M. Magni, M. Milanesi, P. Matteucci, R. Mortarini, A. Anichini, G. Parmiani, et al. 1998. Gene transfer into human dendritic antigen-presenting cells by vaccinia virus and adenovirus vectors. Cancer Gene Ther. 5: 350-356.
11. Zhong, L., A. Granelli-Piperno, Y. Choi, and R. M. Steinman. 1999. Recombinant adenovirus is an efficient and non-perturbing genetic vector for human dendritic cells. Eur. J. Immunol 29: 964-972.
12. Hirschowitz, E. A., J. D. Weaver, G. E. Hidalgo, and D. E. Doherty. 2000. Murine dendritic cells infected with adenovirus vectors show signs of activation. Gene Ther. 7: 1112-1120.
13. Morelli, A. E., A. T. Larregina, R. W. Ganster, A. F. Zahorchak, J. M. Plowey, T. Takayama, A. J. Logar, P. D. Robbins, L. D. Falo, and A. W. Thomson. 2000. Recombinant adenovirus induces maturation of dendritic cells via an NF-κB-dependent pathway. J. Virol 74: 9617-9628.
14. Miller, G., S. Lahrs, A. B. Shah, and R. P. DeMatteo. 2003. Optimization of dendritic cell maturation and gene transfer by recombinant adenovirus. Cancer Immunol. Immunother. 52: 347-358.
15. Molinier-Frenkel, V., R. Lengagne, F. Gaden, S. S. Hong, J. Choppin, H. Gahery-Segard, P. Boulanger, and J. G. Guillet. 2002. Adenovirus hexon protein is a potent adjuvant for activation of a cellular immune response. J. Virol. 76: 127-135.
16. Molinier-Frenkel, V., A. Prevost-Blondel, S. S. Hong, R. Lengagne, S. Boudaly, M. K. Magnusson, P. Boulanger, and J. G. Guillet. 2003. The maturation of murine dendritic cells induced by human adenovirus is mediated by the fiber knob domain. J. Biol. Chem. 278: 37175-37182.
17. Philpott, N. J., M. Nociari, K. B. Elkon, and E. Falck-Pedersen. 2004. Adenovirus-induced maturation of dendritic cells through a PI3 kinase-mediated TNF-α induction pathway. Proc. Natl. Acad. Sci. USA 101: 6200-6205.
18. Takeda, K., and S. Akira. 2005. Toll-like receptors in innate immunity. Int. Immunol. 17: 1-14.
19. Alexopoulou, L., A. C. Holt, R. Medzhitov, and R. A. Flavell. 2001. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 413: 732-738.
20. Heil, F., H. Hemmi, H. Hochrein, F. Ampenberger, C. Kirschning, S. Akira, G. Lipford, H. Wagner, and S. Bauer. 2004. Species-specific recognition of single-stranded RNA via Toll-like receptor 7 and 8. Science 303: 1526-1529.
21. Diebold, S. S., T. Kaisho, H. Hemmi, S. Akira, and C. Reis e Sousa. 2004. Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 303: 1529-1531.
22. Lund, J. M., L. Alexopoulou, A. Sato, M. Karow, N. C. Adams, N. W. Gale, A. Iwasaki, and R. A. Flavell. 2004. Recognition of single-stranded RNA viruses by Toll-like receptor J. Proc. Natl. Acad. Sci. USA 101: 5598-5603.
23. Lund, J., A. Sato, S. Akira, R. Medzhitov, and A. Iwasaki. 2003. Toll-like receptor 9-mediated recognition of Herpes simplex virus-2 by plasmacytoid dendritic cells. J. Exp. Mad. 198: 513-520.
24. Krug, A., G. D. Luker, W. Barchet, D. A. Leib, S. Akira, and M. Colonna. 2004. Herpes simplex virus type 1 activates murine natural interferon-producing cells through Toll-like receptor 9. Blood 103: 1433-1437.
25. Bieback, K., E. Lien, I. M. Klagge, E. Avota, J. Schneider-Schaulies, W. P. Duprex, H. Wagner, C. J. Kirschning, V. Ter Meulen, and S. Schneider-Schaulies. 2002. Hemagglutinin protein of wild-type measles virus activates toll-like receptor 2 signaling. J. Virol. 76: 8729-8736.
26. Kurt-Jones, E. A., L. Popova, L. Kwinn, L. M. Haynes, L. P. Jones, R. A. Tripp, E. E. Walsh, M. W. Freeman, D. T. Golenbock, L. J. Anderson, and R. W. Finberg. 2000. Pattern recognition receptors TLR4 and CD14 mediate response to respiratory syncytial virus. Nat. Immunol. 1: 398-401.
27. Rassa, J. C., J. L. Meyers, Y. Zhang, R. Kudaravalli, and S. R. Ross. 2002. Murine retroviruses activate B cells via interaction with toll-like receptor 4. Proc. Natl. Acad. Sci. USA 99: 2281-2286.
28. Toshchakov, V., B. W. Jones, P. Y. Perera, K. Thomas, M. J. Cody, S. Zhang, B. R. Williams, J. Major, T. A. Hamilton, M. J. Fenton, and S. N. Vogel. 2002. TLR4, but not TLR2, mediates IFN-β-induced STAT1α/β- dependent gene expression in macrophages. Nat. Immunol. 3: 392-398.
29. Doyle, S. E., R. O'Connell, S. A. Vaidya, E. K. Chow, K. Yee, and G. Cheng. 2003. Toll-like receptor 3 mediates a more potent antiviral response than Toll-like receptor 4. J. Immunol. 170: 3565-3571.
30. Sun, S., X. Zhang, D. F. Tough, and J. Sprent. 1998. Type I interferon-mediated stimulation of T cells by CpG DNA. J. Exp. Med. 188: 2335-2342.
31. Muller, U., U. Steinhoff, L. F. Rets, S. Hemmi, J. Pavlovic, R. M. Zinkernagel, and M. Aguet. 1994. Functional role of type I and type II interferons in antiviral defense. Science 264: 1918-1921.
32. Hoebe, K., E. M. Janssen, S. O. Kim, L. Alexopoulou, R. A. Flavell, J. Han, and B. Beutler. 2003. Upregulation of costimulatory molecules induced by lipopolysaccharide and double-stranded RNA occurs by Trif-dependent and Trif-independent pathways. Nat. Immunol. 4: 1223-1229.
33. Honda, K., S. Sakaguchi, C. Nakajima, A. Watanabe, H. Yanai, M. Matsumoto, T. Ohteki, T. Kaisho, A. Takaoka, S. Akira, et al. 2003. Selective contribution of IFN-α/β signaling to the maturation of dendritic cells induced by double-stranded RNA or viral infection. Proc. Natl. Acad. Sci. USA 100: 10872-10877.
34. Pollara, G., M. Jones, M. E. Handley, M. Rajpopat, A. Kwan, R. S. Coffin, G. Foster, B. Chain, and D. R. Katz. 2004. Herpes simplex virus type-1-induced activation of myeloid dendritic cells: the roles of virus cell interaction and paracrine type 1 IFN secretion. J. Immunol. 173: 4108-4119.
35. Montoya, M., M. J. Edwards, D. M. Reid, and P. Borrow. 2005. Rapid activation of spleen dendritic cell subsets following lymphocytic choriomeningitis virus infection of mice: analysis of the involvement of type 1 IFN. J. Immunol. 174: 1851-1861.
36. Lopez, C. B., A. Garcia-Sastre, B. R. Williams, and T. M. Moran. 2003. Type I interferon induction pathway, but not released interferon, participates in the maturation of dendritic cells induced by negative-strand RNA viruses. J. Infect. Dis. 187: 1126-1136.
37. Adachi, O., T. Kawai, K. Takeda, M. Matsumoto, H. Tsutsui, M. Sakagami, K. Nakanishi, and S. Akira. 1998. Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 9: 143-150.
38. + T cells by infected dendritic cells in vivo. Nat. Immunol. 3: 265-271.
39. Xiang, Z. Q., Y. Yang, J. M. Wilson, and H. C. Ertl. 1996. A replication-defective human adenovirus recombinant serves as a highly efficacious vaccine carrier. Virology 219: 220-227.
40. Cotten, M., E. Wagner, K. Zatjoukal, S. Phillips, D. T. Curiel, and M. L. Birnstiel. 1992. High-efficiency receptor-mediated delivery of small and large (48 kilobase gene constructs using the endosome-disruption activity of defective or chemically inactivated adenovirus particles. Proc. Natl. Acad. Sci. USA 89: 6094-6098.
41. Lutz, M. B., N. Kukutsch, A. L. Ogilvie, S. Rossner, F. Koch, N. Romani, and G. Schuler. 1999. An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J. Immunol. Methods 223: 77-92.
42. Asselin-Paturel, C., A. Boonstra, M. Dalod, I. Durand, N. Yessaad, C. Dezutter-Dambuyant, A. Vicari, A. O'Garra, C. Biron, F. Briere, and G. Trinchieri. 2001. Mouse type I IFN-producing cells are immature APCs with plasmacytoid morphology. Nat. Immunol. 2: 1144-1150.
43. Porgador, A., J. W. Yewdell, Y. Deng, J. R. Bennink, and R. N. Germain. 1997. Localization, quantitation, and in situ detection of specific peptide-MHC class I complexes using a monoclonal antibody. Immunity 6: 715-726.
44. Xiang, Z., G. Gao, A. Reyes-Sandoval, C. J. Cohen, Y. Li, J. M. Bergelson, J. M. Wilson, and H. C. Ertl. 2002. Novel, chimpanzee serotype 68-based adenoviral vaccine carrier for induction of antibodies to a transgene product. J. Virol. 76: 2667-2675.
45. Varnavski, A. N., K. Schlienger, J. M. Bergelson, G. P. Gao, and J. M. Wilson. 2003. Efficient transduction of human monocyte-derived dendritic cells by chimpanzee-derived adenoviral vector. Hum. Gene Ther. 14: 533-544.
46. Fields, B. N., D. M. Knipe, P. M. Howley, and D. E. Griffin. 2001. Fields' Virology. Lippincott Williams & Wilkins, Philadelphia.
47. Bergelson, J. M., J. A. Cunningham, G. Droguett, E. A. Kurt-Jones, A. Krithivas, J. S. Hong, M. S. Horwitz, R. L. Crowell, and R. W. Finberg. 1997. Isolation of a common receptor for coxsackie B viruses and adenoviruses 2 and 5. Science 275: 1320-1323.
48. Cohen, C. J., Z. Q. Xiang, G. P. Gao, H. C. Ertl, J. M. Wilson, and J. M. Bergelson. 2002. Chimpanzee adenovirus CV-68 adapted as a gene delivery vector interacts with the coxsackievirus and adenovirus receptor. J. Gen. Virol. 83: 151-155.
49. 5 promote adenovirus internalization but not virus attachment. Cell 73: 309-319.
50. Okada, N., Y. Tsukada, S. Nakagawa, H. Mizuguchi, K. Mori, T. Saito, T. Fujita, A. Yamamoto, T. Hayakawa, and T. Mayumi. 2001. Efficient gene delivery into dendritic cells by fiber-mutant adenovirus vectors. Biochem. Biophys. Res. Commun. 282: 173-179.
51. v integrins requires phosphoinositide-3-OH kinase. J. Virol. 72: 2055-2061.
52. + T cells to an HIV-1 antigen upon oral immunization of mice with a simian E1-deleted adenoviral vector. Vaccine 22: 697-703.
53. Lemiale, F., W. P. Kong, L. M. Akyurek, X. Ling, Y. Huang, B. K. Chakrabarti, M. Eckhaus, and G. J. Nabel. 2003. Enhanced mucosal immunoglobulin A response of intranasal adenoviral vector human immunodeficiency virus vaccine and localization in the central nervous system. J. Virol. 77: 10078-10087.
54. Wherry, E. J., J. N. Blattman, K. Murali-Krishna, R. van der Most, and R. Ahmed. 2003. Viral persistence alters CD8 T-cell immunodominance and tissue distribution and results in distinct stages of functional impairment. J. Virol. 77:4911-4927.
55. + T cells by a flow cytometric assay for degranulation. J Immunol. Methods 281: 65-78.