The effect of adenovirus-specific antibodies on adenoviral vector–induced, transgene product–specific T cell responses

Journal of Leukocyte Biology

Volumn 96, Issue 5, 2014, Pages 821-831

  Small, Juliana C ^a,b   Haut, Larissa H ^a   Bian, Ang ^a   Ertl, Hildegund C J ^a,b  

^a WISTAR INSTITUTE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Adenovirus hexon; AdHu5 immune serum; HIV vaccine; STEP trial; Virus neutralizing antibodies

Indexed keywords

ADENOVIRUS VECTOR; CD8 ANTIGEN; GENOMIC DNA; NEUTRALIZING ANTIBODY; ANTISERUM; EPITOPE; GAG PROTEIN; T LYMPHOCYTE RECEPTOR; VIRUS ANTIBODY;

ADENOVIRIDAE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD8+ T LYMPHOCYTE; CELL EXPANSION; CELL FATE; CONTROLLED STUDY; FEMALE; IMMUNOGENICITY; MEMORY CELL; MOUSE; NONHUMAN; PHASE TRANSITION; SEROTYPE; TRANSGENE; ADENOVIRIDAE INFECTIONS; ANIMAL; ANTIBODY SPECIFICITY; CLASSIFICATION; CROSS REACTION; GENE VECTOR; GENETIC TRANSDUCTION; GENETICS; HUMAN; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; IMMUNOPHENOTYPING; METABOLISM; PASSIVE IMMUNIZATION; PHENOTYPE; T LYMPHOCYTE SUBPOPULATION;

ADENOVIRIDAE; ADENOVIRIDAE INFECTIONS; ANIMALS; ANTIBODIES, VIRAL; ANTIBODY SPECIFICITY; CROSS REACTIONS; EPITOPES; FEMALE; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; GENETIC VECTORS; HUMANS; IMMUNE SERA; IMMUNIZATION, PASSIVE; IMMUNOLOGIC MEMORY; IMMUNOPHENOTYPING; MICE; PHENOTYPE; T-CELL ANTIGEN RECEPTOR SPECIFICITY; T-LYMPHOCYTE SUBSETS; TRANSDUCTION, GENETIC; TRANSGENES;

EID: 84908262416     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.1A0813-451RR     Document Type: Article

References (29)

1. Shiver, J. W., Fu, T.-M., Chen, L., Casimiro, D. R., Davies, M.-E., Evans, R. K., Zhang, Z.-Q., Simon, A. J., Trigona, W. L., Dubey, S. A., Huang, L., Harris, V. A., Long, R. S., Liang, X., Handt, L., Schleif, W. A., Zhu, L., Freed, D. C., Persaud, N. V., Guan, L., Punt, K. S., Tang, A., Chen, M., Wilson, K. A., Collins, K. B., Heidecker, G. J., Fernandez, V. R., Perry, H. C., Joyce, J. G., Grimm, K. M., Cook, J. C., Keller, P. M., Kresock, D. S., Mach, H., Troutman, R. D., Isopi, L. A., Williams, D. M., Xu, Z., Bohannon, K. E., Volkin, D. B., Montefiori, D. C., Miura, A., Krivulka, G. R., Lifton, M. A., Kuroda, M. J., Schmitz, J. E., Letvin, N. L., Caulfield, M. J., Bett, A. J., Youil, R., Kaslow, D. C., Emini, E. A. (2002) Replication-incompetent adenoviral vaccine vector elicits effective antiimmunodeficiency- virus immunity. Nature 415, 331–335.
2. Harro, C. D., Robertson, M. N., Lally, M. A., O’Neill, L. D., Edupuganti, S., Goepfert, P. A., Mulligan, M. J., Priddy, F. H., Dubey, S. A., Kierstead, L. S., Sun, X., Casimiro, D. R., DiNubile, M. J., Shiver, J. W., Leavitt, R. Y., Mehrotra, D. V., Merck V520-007/012 Study Teams. (2009) Safety and immunogenicity of adenovirus-vectored near-consensus HIV type 1 clade B gag vaccines in healthy adults. AIDS Res. Hum. Retroviruses 25, 103–114.
3. McElrath, M. J., De Rosa, S. C., Moodie, Z., Dubey, S., Kierstead, L., Janes, H., Defawe, O. D., Carter, D. K., Hural, J., Akondy, R., Buchbinder, S. P., Robertson, M. N., Mehrotra, D. V., Self, S. G., Corey, L., Shiver, J. W., Casimiro, D. R. (2008) HIV-1 vaccine-induced immunity in the test-of-concept Step Study: a case–cohort analysis. Lancet 372, 1894–1905.
4. Buchbinder, S. P., Mehrotra, D. V., Duerr, A., Fitzgerald, D. W., Mogg, R., Li, D., Gilbert, P. B., Lama, J. R., Marmor, M., del Rio, C., McElrath, M. J., Casimiro, D. R., Gottesdiener, K. M., Chodakewitz, J. A., Corey, L., Robertson, M. N. (2008) Efficacy assessment of a cell-mediated immunity HIV-1 vaccine (the Step Study): a double-blind, randomised, placebo- controlled, test-of-concept trial. Lancet 372, 1881–1893.
5. Xiang, Z., Li, Y., Cun, A., Yang, W., Ellenberg, S., Switzer, W. M., Kalish, M. L., Ertl, H. C. J. (2006) Chimpanzee adenovirus antibodies in humans, sub-Saharan Africa. Emerg. Infect. Dis. 12, 1596–1599.
6. Yang, Y., Li, Q., Ertl, H. C., Wilson, J. M. (1995) Cellular and humoral immune responses to viral antigens create barriers to lung-directed gene therapy with recombinant adenoviruses. J. Virol. 69, 2004–2015.
7. McCoy, K., Tatsis, N., Korioth-Schmitz, B., Lásaro, M. O., Hensley, S. E., Lin, S. W., Li, Y., Giles-Davis, W., Cun, A., Zhou, D., Xiang, Z., Letvin, N. L., Ertl, H. C. J. (2007) Effect of preexisting immunity to adenovirus human serotype 5 antigens on the immune responses of nonhuman primates to vaccine regimens based on human- or chimpanzee-derived adenovirus vectors. J. Virol. 81, 6594–6604.
8. Sumida, S. M., Truitt, D. M., Kishko, M. G., Arthur, J. C., Jackson, S. S., Gorgone, D. A., Lifton, M. A., Koudstaal, W., Pau, M. G., Kostense, S., Havenga, M. J. E., Goudsmit, J., Letvin, N. L., Barouch, D. H. (2004) Neutralizing antibodies and CD8+ T lymphocytes both contribute to immunity to adenovirus serotype 5 vaccine vectors. J. Virol. 78, 2666–2673.
9. Xiang, Z., Gao, G., Reyes-Sandoval, A., Cohen, C. J., Li, Y., Bergelson, J. M., Wilson, J. M., Ertl, H. C. J. (2002) Novel, chimpanzee serotype 68-based adenoviral vaccine carrier for induction of antibodies to a transgene product. J. Virol. 76, 2667–2675.
10. Benlahrech, A., Harris, J., Meiser, A., Papagatsias, T., Hornig, J., Hayes, P., Lieber, A., Athanasopoulos, T., Bachy, V., Csomor, E. (2009) Adenovirus vector vaccination induces expansion of memory CD4 T cells with a mucosal homing phenotype that are readily susceptible to HIV-1. Proc. Natl. Acad. Sci. U. S. A. 106, 19940–19945.
11. Perreau, M., Pantaleo, G., Kremer, E. J. (2008) Activation of a dendritic cell-T cell axis by Ad5 immune complexes creates an improved environment for replication of HIV in T cells. J. Exp. Med. 205, 2717–2725.
12. Seshidhar Reddy, P., Ganesh, S., Limbach, M. P., Brann, T., Pinkstaff, A., Kaloss, M., Kaleko, M., Connelly, S. (2003) Development of adenovirus serotype 35 as a gene transfer vector. Virology 311, 384–393.
13. Barouch, D. H., Liu, J., Peter, L., Abbink, P., Iampietro, M. J., Cheung, A., Alter, G., Chung, A., Dugast, A. S., Frahm, N., McElrath, M. J., Wenschuh, H., Reimer, U., Seaman, M. S., Pau, M. G., Weijtens, M., Goudsmit, J., Walsh, S. R., Dolin, R., Baden, L. R. (2012) Characterization of humoral and cellular immune responses elicited by a recombinant adenovirus serotype 26 HIV-1 env vaccine in healthy adults (IPCAVD 001). J. Infect. Dis. 207, 248–256.
14. Lasaro, M. O., Ertl, H. C. (2009) New insights on adenovirus as vaccine vectors. Mol. Ther. 17, 1333–1339.
15. Barouch, D. H., Kik, S. V., Weverling, G. J., Dilan, R., King, S. L., Maxfield, L. F., Clark, S., Ng’ang’a, D., Brandariz, K. L., Abbink, P., Sinangil, F., de Bruyn, G., Gray, G. E., Roux, S., Bekker, L.-G., Dilraj, A., Kibuuka, H., Robb, M. L., Michael, N. L., Anzala, O., Amornkul, P. N., Gilmour, J., Hural, J., Buchbinder, S. P., Seaman, M. S., Dolin, R., Baden, L. R., Carville, A., Mansfield, K. G., Pau, M. G., Goudsmit, J. (2011) International seroepidemiology of adenovirus serotypes 5, 26, 35, and 48 in pediatric and adult populations. Vaccine 29, 5203–5209.
16. Chen, H., Xiang, Z. Q., Li, Y., Kurupati, R. K., Jia, B., Bian, A., Zhou, D. M., Hutnick, N., Yuan, S., Gray, C., Serwanga, J., Auma, B., Kaleebu, P., Zhou, X., Betts, M. R., Ertl, H. C. J. (2010) Adenovirus-based vaccines: comparison of vectors from three species of Adenoviridae. J. Virol. 84, 10522–10532.
17. Zhou, D., Zhou, X., Bian, A., Li, H., Chen, H., Small, J. C., Li, Y., Giles- Davis, W., Xiang, Z., Ertl, H. C. J. (2010) An efficient method of directly cloning chimpanzee adenovirus as a vaccine vector. Nat. Protoc. 5, 1775–1785.
18. Haut, L. H., Lin, S. W., Tatsis, N., DiMenna, L. J., Giles-Davis, W., Pinto, A. R., Ertl, H. C. J. (2010) Robust genital gag-specific CD8+ T cell responses in mice upon intramuscular immunization with simian adenoviral vectors expressing HIV-1-gag. Eur. J. Immunol. 40, 3426–3438.
19. Tatsis, N., Fitzgerald, J. C., Reyes-Sandoval, A., Harris-McCoy, K. C., Hensley, S. E., Zhou, D., Lin, S. W., Bian, A., Xiang, Z. Q., Iparraguirre, A., Lopez-Camacho, C., Wherry, E. J., Ertl, H. C. J. (2007) Adenoviral vectors persist in vivo and maintain activated CD8+ T cells: implications for their use as vaccines. Blood 110, 1916–1923.
20. Sarkar, S., Kalia, V., Haining, W. N., Konieczny, B. T., Subramaniam, S., Ahmed, R. (2008) Functional and genomic profiling of effector CD8 T cell subsets with distinct memory fates. J. Exp. Med. 205, 625–640.
21. Kaech, S. M., Tan, J. T., Wherry, E. J., Konieczny, B. T., Surh, C. D., Ahmed, R. (2003) Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nat. Immunol. 4, 1191–1198.
22. Sallusto, F., Langenkamp, A., Geginat, J., Lanzavecchia, A. (2000) Functional subsets of memory T cells identified by CCR7 expression. Curr. Top. Microbiol. Immunol. 251, 167–171.
23. Willcox, N., Mautner, V. (1976) Antigenic determinants of adenovirus capsids. II. Homogeneity of hexons, and accessibility of their determinants, in the virion. J. Immunol. 116, 25–29.
24. Hensley, S. E., Giles-Davis, W., McCoy, K. C., Weninger, W., Ertl, H. C. (2005) Dendritic cell maturation, but not CD8+ T cell induction, is dependent on type I IFN signaling during vaccination with adenovirus vectors. J. Immunol. 175, 6032–6041.
25. Obar, J. J., Lefrancois, L. (2010) Early signals during CD8+ T cell priming regulate the generation of central memory cells. J. Immunol. 185, 263–272.
26. Garnett, C. T., Erdman, D., Xu, W., Gooding, L. R. (2002) Prevalence and quantitation of species C adenovirus DNA in human mucosal lymphocytes. J. Virol. 76, 10608–10616.
27. Hansen, S. G., Ford, J. C., Lewis, M. S., Ventura, A. B., Hughes, C. M., Coyne-Johnson, L., Whizin, N., Oswald, K., Shoemaker, R., Swanson, T., Legasse, A. W., Chiuchiolo, M. J., Parks, C. L., Axthelm, M. K., Nelson, J. A., Jarvis, M. A., Piatak, M., Lifson, J. D., Picker, L. J. (2012) Profound early control of highly pathogenic SIV by an effector memory T cell vaccine. Nature 473, 523–527.
28. Vaccari, M., Trindade, C. J., Venzon, D., Zanetti, M., Franchini, G. (2005) Vaccine-induced CD8+ central memory T cells in protection from simian AIDS. J. Immunol. 175, 3502–3507.
29. Bachmann, M. F., Wolint, P., Schwarz, K., Oxenius, A. (2005) Recall proliferation potential of memory CD8+ T cells and antiviral protection. J. Immunol. 175, 4677–4685.