Modification of antigen impacts on memory quality after adenovirus vaccination

Journal of Immunology

Volumn 196, Issue 8, 2016, Pages 3354-3363

  Colston, Julia M ^a   Bolinger, Beatrice ^a   Cottingham, Matthew G ^b   Gilbert, Sarah ^b   Klenerman, Paul ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VACCINE; ADENOVIRUS VECTOR; BETA GALACTOSIDASE; EPITOPE; POLYPEPTIDE; ANTIGEN;

ADENOVIRUS VACCINATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTATION; ARTICLE; AVIADENOVIRUS; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOMEGALOVIRUS; GENE VECTOR; MEMORY T LYMPHOCYTE; MINIGENE VECTOR; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; TRANSGENE; VACCINATION; ADENOVIRIDAE; ANIMAL; C57BL MOUSE; CYTOMEGALOVIRUS INFECTION; FEMALE; GENETICS; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; LACTOSE OPERON; MOUSE; VIROLOGY;

ADENOVIRIDAE; ANIMALS; ANTIGENS; CD8-POSITIVE T-LYMPHOCYTES; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; EPITOPES, T-LYMPHOCYTE; FEMALE; IMMUNOLOGIC MEMORY; LAC OPERON; MICE; MICE, INBRED C57BL; PROMOTER REGIONS, GENETIC; TRANSGENES; VACCINATION;

EID: 84974795016     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1502687     Document Type: Article

References (44)

1. Karrer, U., S. Sierro, M. Wagner, A. Oxenius, H. Hengel, U. H. Koszinowski, R. E. Phillips, and P. Klenerman. 2003. Memory inflation: continuous accumulation of antiviral CD8+ T cells over time. J. Immunol. 170: 2022-2029.
2. Munks, M. W., K. S. Cho, A. K. Pinto, S. Sierro, P. Klenerman, and A. B. Hill. 2006. Four distinct patterns of memory CD8 T cell responses to chronic murine cytomegalovirus infection. J. Immunol. 177: 450-458.
3. Komatsu, H., S. Sierro, A. V Cuero, and P. Klenerman. 2003. Population analysis of antiviral T cell responses using MHC class I-peptide tetramers. Clin. Exp. Immunol. 134: 9-12.
4. Gillespie, G. M., M. R. Wills, V. Appay, C. O'Callaghan, M. Murphy, N. Smith, P. Sissons, S. Rowland-Jones, J. I. Bell, and P. A. Moss. 2000. Functional heterogeneity and high frequencies of cytomegalovirus-specific CD8+ T lymphocytes in healthy seropositive donors. J. Virol. 74: 8140-8150.
5. Holtappels, R., M. F. Pahl-Seibert, D. Thomas, and M. J. Reddehase. 2000. Enrichment of immediate-early 1 (m123/pp89) peptide-specific CD8 T cells in a pulmonary CD62Llo memory-effector cell pool during latent murine cytomegalovirus infection of the lungs. J. Virol. 74: 11495-11503.
6. O'Hara, G. A., S. P. Welten, P. Klenerman, and R. Arens. 2012. Memory T cell inflation: understanding cause and effect. Trends Immunol. 33: 84-90.
7. Sierro, S., R. Rothkopf, and P. Klenerman. 2005. Evolution of diverse antiviral CD8+ T cell populations after murine cytomegalovirus infection. Eur. J. Immunol. 35: 1113-1123.
8. Gallimore, A., A. Glithero, A. Godkin, A. C. Tissot, A. Plückthun, T. Elliott, H. Hengartner, and R. Zinkernagel. 1998. Induction and exhaustion of lymphocytic choriomeningitis virus-specific cytotoxic T lymphocytes visualized using soluble tetrameric major histocompatibility complex class I-peptide complexes. J. Exp. Med. 187: 1383-1393.
9. Zajac, A. J., J. N. Blattman, K. Murali-Krishna, D. J. Sourdive, M. Suresh, J. D. Altman, and R. Ahmed. 1998. Viral immune evasion due to persistence of activated T cells without effector function. J. Exp. Med. 188: 2205-2213.
10. Hutchinson, S., S. Sims, G. O'Hara, J. Silk, U. Gileadi, V. Cerundolo, and P. Klenerman. 2011. A dominant role for the immunoproteasome in CD8+ T cell responses to murine cytomegalovirus. PLoS One 6: e14646.
11. Torti, N., S. M. Walton, T. Brocker, T. Rülicke, and A. Oxenius. 2011. Nonhematopoietic cells in lymph nodes drive memory CD8 T cell inflation during murine cytomegalovirus infection. PLoS Pathog. 7: e1002313.
12. Smith, C. J., H. Turula, and C. M. Snyder. 2014. Systemic hematogenous maintenance of memory inflation by MCMV infection. PLoS Pathog. 10: e1004233.
13. Bolinger, B., S. Sims, G. O'Hara, C. de Lara, E. Tchilian, S. Firner, D. Engeler, B. Ludewig, and P. Klenerman. 2013. A new model for CD8+ T cell memory inflation based upon a recombinant adenoviral vector. J. Immunol. 190: 4162-4174.
14. Overwijk, W. W., D. R. Surman, K. Tsung, and N. P. Restifo. 1997. Identification of a Kb-restricted CTL epitope of b-galactosidase: potential use in development of immunization protocols for "self" antigens. Methods 12: 117-123.
15. Oukka, M., M. Cohen-Tannoudji, Y. Tanaka, C. Babinet, and K. Kosmatopoulos. 1996. Medullary thymic epithelial cells induce tolerance to intracellular proteins. J. Immunol. 156: 968-975.
16. Holst, P. J., C. Ørskov, A. R. Thomsen, and J. P. Christensen. 2010. Quality of the transgene-specific CD8+ T cell response induced by adenoviral vector immunization is critically influenced by virus dose and route of vaccination. J. Immunol. 184: 4431-4439.
17. Krebs, P., E. Scandella, B. Odermatt, and B. Ludewig. 2005. Rapid functional exhaustion and deletion of CTL following immunization with recombinant adenovirus. J. Immunol. 174: 4559-4566.
18. Finn, J. D., J. Bassett, J. B. Millar, N. Grinshtein, T. C. Yang, R. Parsons, C. Evelegh, Y. Wan, R. J. Parks, and J. L. Bramson. 2009. Persistence of transgene expression influences CD8+ T-cell expansion and maintenance following immunization with recombinant adenovirus. J. Virol. 83: 12027-12036.
19. Bassett, J. D., T. C. Yang, D. Bernard, J. B. Millar, S. L. Swift, A. J. McGray, H. VanSeggelen, J. E. Boudreau, J. D. Finn, R. Parsons, et al. 2011. CD8+ T-cell expansion and maintenance after recombinant adenovirus immunization rely upon cooperation between hematopoietic and nonhematopoietic antigenpresenting cells. Blood 117: 1146-1155.
20. Bolinger, B., S. Sims, L. Swadling, G. O'Hara, C. de Lara, D. Baban, N. Saghal, L. N. Lee, E. Marchi, M. Davis, et al. 2015. Adenoviral vector vaccination induces a conserved program of CD8 T cell memory differentiation in mouse and man. Cell Rep. 13: 1578-1588.
21. Barnes, E., A. Folgori, S. Capone, L. Swadling, S. Aston, A. Kurioka, J. Meyer, R. Huddart, K. Smith, R. Townsend, et al. 2012. Novel adenovirus-based vaccines induce broad and sustained T cell responses to HCV in man. Sci. Transl. Med. 4: 115ra1.
22. Green, C. A., E. Scarselli, C. J. Sande, A. J. Thompson, C. M. de Lara, K. S. Taylor, K. Haworth, M. Del Sorbo, B. Angus, L. Siani, et al. 2015. Chimpanzee adenovirus-and MVA-vectored respiratory syncytial virus vaccine is safe and immunogenic in adults. Sci. Transl. Med. 7: 300ra126.
23. Ledgerwood, J. E., A. D. DeZure, D. A. Stanley, L. Novik, M. E. Enama, N. M. Berkowitz, Z. Hu, G. Joshi, A. Ploquin, S. Sitar, et al; the VRC 207 Study Team. 2014. Chimpanzee adenovirus vector Ebola vaccine-preliminary report. N. Engl. J. Med.
24. Arita, E., M. Kondoh, K. Isoda, H. Nishimori, T. Yoshida, H. Mizuguchi, and K. Yagi. 2008. Evaluation of promoter strength in mouse and rat primary hepatocytes using adenovirus vectors. Eur. J. Pharm. Biopharm. 70: 1-6.
25. Zheng, C., and B. J. Baum. 2005. Evaluation of viral and mammalian promoters for use in gene delivery to salivary glands. Mol. Ther. 12: 528-536.
26. Chen, P., J. Tian, I. Kovesdi, and J. T. Bruder. 2008. Promoters influence the kinetics of transgene expression following adenovector gene delivery. J. Gene Med. 10: 123-131.
27. Yamamoto, T., B. de Crombrugghe, and I. Pastan. 1980. Identification of a functional promoter in the long terminal repeat of Rous sarcoma virus. Cell 22: 787-797.
28. Kim, D. W., T. Uetsuki, Y. Kaziro, N. Yamaguchi, and S. Sugano. 1990. Use of the human elongation factor 1a promoter as a versatile and efficient expression system. Gene 91: 217-223.
29. Uetsuki, T., A. Naito, S. Nagata, and Y. Kaziro. 1989. Isolation and characterization of the human chromosomal gene for polypeptide chain elongation factor-1a. J. Biol. Chem. 264: 5791-5798.
30. Mizushima, S., and S. Nagata. 1990. pEF-BOS, a powerful mammalian expression vector. Nucleic Acids Res. 18: 5322.
31. Fehling, H. J., W. Swat, C. Laplace, R. Kühn, K. Rajewsky, U. Müller, and H. von Boehmer. 1994. MHC class I expression in mice lacking the proteasome subunit LMP-7. Science 265: 1234-1237.
32. Gilbert, S. C., J. Schneider, C. M. Hannan, J. T. Hu, M. Plebanski, R. Sinden, and A. V. Hill. 2002. Enhanced CD8 T cell immunogenicity and protective efficacy in a mouse malaria model using a recombinant adenoviral vaccine in heterologous prime-boost immunisation regimes. Vaccine 20: 1039-1045.
33. Zarrin, A. A., L. Malkin, I. Fong, K. D. Luk, A. Ghose, and N. L. Berinstein. 1999. Comparison of CMV, RSV, SV40 viral and Vl1 cellular promoters in B and T lymphoid and non-lymphoid cell lines. Biochim. Biophys. Acta 1446: 135-139.
34. Schaack, J., M. L. Bennett, G. S. Shapiro, J. DeGregori, J. L. McManaman, and J. W. Moorhead. 2011. Strong foreign promoters contribute to innate inflammatory responses induced by adenovirus transducing vectors. Virology 412: 28-35.
35. Qin, J. Y., L. Zhang, K. L. Clift, I. Hulur, A. P. Xiang, B. Z. Ren, and B. T. Lahn. 2010. Systematic comparison of constitutive promoters and the doxycyclineinducible promoter. PLoS One 5: e10611.
36. Bachmann, M. F., P. Wolint, K. Schwarz, P. Jäger, and A. Oxenius. 2005. Functional properties and lineage relationship of CD8+ T cell subsets identified by expression of IL-7 receptor a and CD62L. J. Immunol. 175: 4686-4696.
37. Sridhar, S., A. Reyes-Sandoval, S. J. Draper, A. C. Moore, S. C. Gilbert, G. P. Gao, J. M. Wilson, and A. V. Hill. 2008. Single-dose protection against Plasmodium berghei by a simian adenovirus vector using a human cytomegalovirus promoter containing intron A. J. Virol. 82: 3822-3833.
38. Draper, S. J., S. Biswas, A. J. Spencer, E. J. Remarque, S. Capone, M. Naddeo, M. D. Dicks, B. W. Faber, S. C. de Cassan, A. Folgori, et al. 2010. Enhancing blood-stage malaria subunit vaccine immunogenicity in rhesus macaques by combining adenovirus, poxvirus, and protein-in-adjuvant vaccines. J. Immunol. 185: 7583-7595.
39. Swadling, L., S. Capone, R. D. Antrobus, A. Brown, R. Richardson, E. W. Newell, J. Halliday, C. Kelly, D. Bowen, J. Fergusson, et al. 2014. A human vaccine strategy based on chimpanzee adenoviral and MVA vectors that primes, boosts, and sustains functional HCV-specific T cell memory. Sci. Transl. Med. 6: 261ra153.
40. Hansen, S. G., J. C. Ford, M. S. Lewis, A. B. Ventura, C. M. Hughes, L. Coyne-Johnson, N. Whizin, K. Oswald, R. Shoemaker, T. Swanson, et al. 2011. Profound early control of highly pathogenic SIV by an effector memory T-cell vaccine. Nature 473: 523-527.
41. Hodgson, S. H., K. J. Ewer, C. M. Bliss, N. J. Edwards, T. Rampling, N. A. Anagnostou, E. de Barra, T. Havelock, G. Bowyer, I. D. Poulton, et al. 2015. Evaluation of the efficacy of ChAd63-MVA vectored vaccines expressing circumsporozoite protein and ME-TRAP against controlled human malaria infection in malaria-naive individuals. J. Infect. Dis. 211: 1076-1086.
42. Lubaroff, D. M., B. R. Konety, B. Link, J. Gerstbrein, T. Madsen, M. Shannon, J. Howard, J. Paisley, D. Boeglin, T. L. Ratliff, and R. D.Williams. 2009. Phase I clinical trial of an adenovirus/prostate-specific antigen vaccine for prostate cancer: safety and immunologic results. Clin. Cancer Res. 15: 7375-7380.
43. Chapman, B. S., R. M. Thayer, K. A. Vincent, and N. L. Haigwood. 1991. Effect of intron A from human cytomegalovirus (Towne) immediate-early gene on heterologous expression in mammalian cells. Nucleic Acids Res. 19: 3979-3986.
44. Shastri, N., S. Schwab, and T. Serwold. 2002. Producing nature's gene-chips: the generation of peptides for display by MHC class I molecules. Annu. Rev. Immunol. 20: 463-493.