Vaccine vectors derived from a large collection of simian adenoviruses induce potent cellular immunity across multiple species

Science Translational Medicine

Volumn 4, Issue 115, 2012, Pages

  Colloca, Stefano ^a   Barnes, Eleanor ^b,c   Folgori, Antonella ^a   Ammendola, Virginia ^a   Capone, Stefania ^a   Cirillo, Agostino ^d,g   Siani, Loredana ^a   Naddeo, Mariarosaria ^a   Grazioli, Fabiana ^a   Esposito, Maria Luisa ^a   Ambrosio, Maria ^a   Sparacino, Angela ^a   Bartiromo, Marta ^a   Meola, Annalisa ^d   Smith, Kira ^b   Kurioka, Ayako ^b   O'Hara, Geraldine A ^e   Ewer, Katie J ^e   Anagnostou, Nicholas ^e   Bliss, Carly ^e   Hill, Adrian V S ^e   Traboni, Cinzia ^a   Klenerman, Paul ^b   Cortese, Riccardo ^a,f   Nicosia, Alfredo ^a,f   more..

^a Okairos ^*  (Italy)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c JOHN RADCLIFFE HOSPITAL   (United Kingdom)

^d IRBM   (Italy)

^e UNIVERSITY OF OXFORD   (United Kingdom)

^f CEINGE BIOTECNOLOGIE AVANZATE   (Italy)

^g NOVARTIS PHARMA AG   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE; ADENOVIRUS VECTOR; GUANOSINE; NEUTRALIZING ANTIBODY; THYMINE; VIRUS VECTOR; GAMMA INTERFERON;

ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CROSS REACTION; FEMALE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; MEMORY CELL; MOUSE; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; SEROPREVALENCE; SEROTYPE; SIMIAN VIRUS; T LYMPHOCYTE; VIRUS REPLICATION; VIRUS STRAIN; ADENOVIRUS; ANIMAL; CELL LINE; DOSE RESPONSE; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE VECTOR; GENETICS; IMMUNE SYSTEM; IMMUNOLOGY; METABOLISM; METHODOLOGY; PAN TROGLODYTES; SPECIES DIFFERENCE; VIROLOGY;

ADENOVIRIDAE; ADENOVIRUSES, SIMIAN; ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENETIC VECTORS; HUMANS; IMMUNE SYSTEM; IMMUNITY, CELLULAR; INTERFERON-GAMMA; MICE; PAN TROGLODYTES; PHYLOGENY; SPECIES SPECIFICITY;

EID: 84855372641     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3002925     Document Type: Article

References (38)

1. P. S. Kim, R. Ahmed, Features of responding T cells in cancer and chronic infection. Curr. Opin. Immunol. 22, 223-230 (2010).
2. D. H. Barouch, Novel adenovirus vector-based vaccines for HIV-1. Curr. Opin. HIV AIDS 5, 386-390 (2010).
3. D. R. Casimiro, L. Chen, T. M. Fu, R. K. Evans, M. J. Caulfield, M. E. Davies, A. Tang, M. Chen, L. Huang, V. Harris, D. C. Freed, K. A. Wilson, S. Dubey, D. M. Zhu, D. Nawrocki, H. Mach, R. Troutman, L. Isopi, D. Williams, W. Hurni, Z. Xu, J. G. Smith, S. Wang, X. Liu, L. Guan, R. Long, W. Trigona, G. J. Heidecker, H. C. Perry, N. Persaud, T. J. Toner, Q. Su, X. Liang, R. Youil, M. Chastain, A. J. Bett, D. B. Volkin, E. A. Emini, J. W. Shiver, Comparative immunogenicity in rhesus monkeys of DNA plasmid, recombinant vaccinia virus, and replication-defective adenovirus vectors expressing a human immunodeficiency virus type 1 gag gene. J. Virol. 77, 6305-6313 (2003).
4. C. Harro, X. Sun, J. E. Stek, R. Y. Leavitt, D. V. Mehrotra, F. Wang, A. J. Bett, D. R. Casimiro, J. W. Shiver, M. J. DiNubile, E. Quirk; Merck V526-001 Study Group, Safety and immunogenicity of the Merck adenovirus serotype 5 (MRKAd5) and MRKAd6 human immunodeficiency virus type 1 trigene vaccines alone and in combination in healthy adults. Clin. Vaccine Immunol. 16, 1285-1292 (2009).
5. J. E. Ledgerwood, P. Costner, N. Desai, L. Holman, M. E. Enama, G. Yamshchikov, S. Mulangu, Z. Hu, C. A. Andrews, R. A. Sheets, R. A. Koup, M. Roederer, R. Bailer, J. R. Mascola, M. G. Pau, N. J. Sullivan, J. Goudsmit, G. J. Nabel, B. S. Graham; VRC 205 Study Team, A replication defective recombinant Ad5 vaccine expressing Ebola virus GP is safe and immunogenic in healthy adults. Vaccine 29, 304-313 (2010).
6. J. Liu, K. L. O'Brien, D. M. Lynch, N. L. Simmons, A. La Porte, A. M. Riggs, P. Abbink, R. T. Coffey, L. E. Grandpre, M. S. Seaman, G. Landucci, D. N. Forthal, D. C. Montefiori, A. Carville, K. G. Mansfield, M. J. Havenga, M. G. Pau, J. Goudsmit, D. H. Barouch, Immune control of an SIV challenge by a T-cell-based vaccine in rhesus monkeys. Nature 457, 87-91 (2009).
7. N. Tatsis, H. C. Ertl, Adenoviruses as vaccine vectors. Mol. Ther. 10, 616-629 (2004).
8. A. T. Catanzaro, R. A. Koup, M. Roederer, R. T. Bailer, M. E. Enama, Z. Moodie, L. Gu, J. E. Martin, L. Novik, B. K. Chakrabarti, B. T. Butman, J. G. Gall, C. R. King, C. A. Andrews, R. Sheets, P. L. Gomez, J. R. Mascola, G. J. Nabel, B. S. Graham; Vaccine Research Center Study Team, Phase 1 safety and immunogenicity evaluation of a multiclade HIV-1 candidate vaccine delivered by a replication-defective recombinant adenovirus vector. J. Infect. Dis. 194, 1638-1649 (2006).
9. F. H. Priddy, D. Brown, J. Kublin, K. Monahan, D. P.Wright, J. Lalezari, S. Santiago, M.Marmor, M. Lally, R. M. Novak, S. J. Brown, P. Kulkarni, S. A. Dubey, L. S. Kierstead, D. R. Casimiro, R. Mogg, M. J. DiNubile, J. W. Shiver, R. Y. Leavitt, M. N. Robertson, D. V. Mehrotra, E. Quirk; Merck V520-016 Study Group, Safety and immunogenicity of a replication-incompetent adenovirus type 5 HIV-1 clade B gag/pol/nef vaccine in healthy adults. Clin. Infect. Dis. 46, 1769-1781 (2008).
10. M. J. McElrath, S. C. De Rosa, Z. Moodie, S. Dubey, L. Kierstead, H. Janes, O. D. Defawe, D. K. Carter, J. Hural, R. Akondy, S. P. Buchbinder, M. N. Robertson, D. V. Mehrotra, S. G. Self, L. Corey, J. W. Shiver, D. R. Casimiro; Step Study Protocol Team, HIV-1 vaccine-induced immunity in the test-of-concept Step Study: A case-cohort analysis. Lancet 372, 1894-1905 (2008).
11. S. P. Buchbinder, D. V. Mehrotra, A. Duerr, D.W. Fitzgerald, R. Mogg, D. Li, P. B. Gilbert, J. R. Lama, M. Marmor, C. Del Rio, M. J. McElrath, D. R. Casimiro, K. M. Gottesdiener, J. A. Chodakewitz, L. Corey, M. N. Robertson; Step Study Protocol Team, 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 (2008).
12. P. Abbink, A. A. Lemckert, B. A. Ewald, D. M. Lynch, M. Denholtz, S. Smits, L. Holterman, I. Damen, R. Vogels, A. R. Thorner, K. L. O'Brien, A. Carville, K. G. Mansfield, J. Goudsmit, M. J. Havenga, D. H. Barouch, Comparative seroprevalence and immunogenicity of six rare serotype recombinant adenovirus vaccine vectors from subgroups B and D. J. Virol. 81, 4654-4663 (2007).
13. A. A. Lemckert, S. M. Sumida, L. Holterman, R. Vogels, D. M. Truitt, D. M. Lynch, A. Nanda, B. A. Ewald, D. A. Gorgone, M. A. Lifton, J. Goudsmit, M. J. Havenga, D. H. Barouch, Immunogenicity of heterologous prime-boost regimens involving recombinant adenovirus serotype 11 (Ad11) and Ad35 vaccine vectors in the presence of anti-ad5 immunity. J. Virol. 79, 9694-9701 (2005).
14. J. Liu, B. A. Ewald, D. M. Lynch, M. Denholtz, P. Abbink, A. A. Lemckert, A. Carville, K. G. Mansfield, M. J. Havenga, J. Goudsmit, D. H. Barouch, Magnitude and phenotype of cellular immune responses elicited by recombinant adenovirus vectors and heterologous prime-boost regimens in rhesus monkeys. J. Virol. 82, 4844-4852 (2008).
15. K. Radosevic, A. Rodriguez, A. A. Lemckert, M. van der Meer, G. Gillissen, C. Warnar, R. von Eyben, M. G. Pau, J. Goudsmit, The Th1 immune response to Plasmodium falciparum circumsporozoite protein is boosted by adenovirus vectors 35 and 26 with a homologous insert. Clin. Vaccine Immunol. 17, 1687-1694 (2010).
16. T. W. Geisbert, M. Bailey, L. Hensley, C. Asiedu, J. Geisbert, D. Stanley, A. Honko, J. Johnson, S. Mulangu, M. G. Pau, J. Custers, J. Vellinga, J. Hendriks, P. Jahrling, M. Roederer, J. Goudsmit, R. Koup, N. J. Sullivan, Recombinant adenovirus serotype 26 (Ad26) and Ad35 vaccine vectors bypass immunity to Ad5 and protect nonhuman primates against ebolavirus challenge. J. Virol. 85, 4222-4233 (2011).
17. M. Horowitz, Adenoviridae and Their Replication (Raven Press, New York, 1990), pp. 1679-1740.
18. H. Chen, Z. Q. Xiang, Y. Li, R. K. Kurupati, B. Jia, A. Bian, D. M. Zhou, N. Hutnick, S. Yuan, C. Gray, J. Serwanga, B. Auma, P. Kaleebu, X. Zhou, M. R. Betts, H. C. Ertl, Adenovirus-based vaccines: Comparison of vectors from three species of adenoviridae. J. Virol. 84, 10522-10532 (2010).
19. S. Roy, L. H. Vandenberghe, S. Kryazhimskiy, R. Grant, R. Calcedo, X. Yuan, M. Keough, A. Sandhu, Q. Wang, C. A. Medina-Jaszek, J. B. Plotkin, J. M. Wilson, Isolation and characterization of adenoviruses persistently shed from the gastrointestinal tract of non-human primates. PLoS Pathog. 5, e1000503 (2009).
20. S. Capone, I. Zampaglione, A. Vitelli, M. Pezzanera, L. Kierstead, J. Burns, L. Ruggeri, M. Arcuri, M. Cappelletti, A. Meola, B. B. Ercole, R. Tafi, C. Santini, A. Luzzago, T. M. Fu, S. Colloca, G. Ciliberto, R. Cortese, A. Nicosia, E. Fattori, A. Folgori, Modulation of the immune response induced by gene electrotransfer of a hepatitis C virus DNA vaccine in nonhuman primates. J. Immunol. 177, 7462-7471 (2006).
21. A. Folgori, S. Capone, L. Ruggeri, A. Meola, E. Sporeno, B. B. Ercole, M. Pezzanera, R. Tafi, M. Arcuri, E. Fattori, A. Lahm, A. Luzzago, A. Vitelli, S. Colloca, R. Cortese, A. Nicosia, A T-cell HCV vaccine eliciting effective immunity against heterologous virus challenge in chimpanzees. Nat. Med. 12, 190-197 (2006).
22. S. Capone, A. Meola, B. B. Ercole, A. Vitelli, M. Pezzanera, L. Ruggeri, M. E. Davies, R. Tafi, C. Santini, A. Luzzago, T. M. Fu, A. Bett, S. Colloca, R. Cortese, A. Nicosia, A. Folgori, A novel adenovirus type 6 (Ad6)-based hepatitis C virus vector that overcomes preexisting anti-ad5 immunity and induces potent and broad cellular immune responses in rhesus macaques. J. Virol. 80, 1688-1699 (2006).
23. E. Barnes, A. Folgori, S. Capone, L. Swadling, S. Aston, A. Kurioka, J. Meyer, R. Huddart, K. Smith, R. Townsend, A. Brown, R. Antrobus, V. Ammendola, M. Naddeo, G. O'Hara, C. Willberg, A. Harrison, F. Grazioli, M. L. Esposito, L. Siani, C. Traboni, Y. Oo, D. Adams, A. V. S. Hill, S. Colloca, A. Nicosia, R. Cortese, P. Klenerman, Novel adenovirus-based vaccines induce broad and sustained T cell responses to HCV in man. Sci. Transl. Med. 4, 115ra1 (2012).
24. S. Capone, A. Reyes-Sandoval, M. Naddeo, L. Siani, V. Ammendola, C. S. Rollier, A. Nicosia, S. Colloca, R. Cortese, A. Folgori, A. V. Hill, Immune responses against a liver-stage malaria antigen induced by simian adenoviral vector AdCh63 and MVA prime-boost immunisation in non-human primates. Vaccine 29, 256-265 (2010).
25. M. Dudareva, L. Andrews, S. C. Gilbert, P. Bejon, K. Marsh, J. Mwacharo, O. Kai, A. Nicosia, A. V. Hill, Prevalence of serum neutralizing antibodies against chimpanzee adenovirus 63 and human adenovirus 5 in Kenyan children, in the context of vaccine vector efficacy. Vaccine 27, 3501-3504 (2009).
26. + T-cell responses. Infect. Immun. 78, 145-153 (2010).
27. http://www.hvtn.org/meeting/ppt/may10/2/P3/DeRosa-HVTN077.pdf
28. S. F. Farina, G. P. Gao, Z. Q. Xiang, J. J. Rux, R. M. Burnett, M. R. Alvira, J. Marsh, H. C. Ertl, J. M. Wilson, Replication-defective vector based on a chimpanzee adenovirus. J. Virol. 75, 11603-11613 (2001).
29. S. Roy, A. Medina-Jaszek, M. J. Wilson, A. Sandhu, R. Calcedo, J. Lin, J. M. Wilson, Creation of a panel of vectors based on ape adenovirus isolates. J. Gene Med. 13, 17-25 (2011).
30. H. Kaessmann, V. Wiebe, S. Pääbo, Extensive nuclear DNA sequence diversity among chimpanzees. Science 286, 1159-1162 (1999).
31. H. Kaessmann, V. Wiebe, G. Weiss, S. Pääbo, Great ape DNA sequences reveal a reduced diversity and an expansion in humans. Nat. Genet. 27, 155-156 (2001).
32. W. Liu, Y. Li, G. H. Learn, R. S. Rudicell, J. D. Robertson, B. F. Keele, J. B. Ndjango, C. M. Sanz, D. B. Morgan, S. Locatelli, M. K. Gonder, P. J. Kranzusch, P. D.Walsh, E. Delaporte, E.Mpoudi-Ngole, A. V. Georgiev, M. N. Muller, G. M. Shaw, M. Peeters, P. M. Sharp, J. C. Rayner, B. H. Hahn, Origin of the human malaria parasite Plasmodium falciparum in gorillas. Nature 467, 420-425 (2010).
33. S. J. Draper, S. Biswas, A. J. Spencer, E. J. Remarque, S. Capone, M. Naddeo, M. D. Dicks, B. W. Faber, S. C. de Cassan, A. Folgori, A. Nicosia, S. C. Gilbert, A. V. Hill, Enhancing blood-stage malaria subunit vaccine immunogenicity in rhesus macaques by combining adenovirus, poxvirus, and protein-in-adjuvant vaccines. J. Immunol. 185, 7583-7595 (2010).
34. + dendritic cells but show redundancy in their requirement of TLR and nucleotide-binding oligomerization domain-like receptor signaling. J. Immunol. 185, 1513-1521 (2010).
35. N. Arnberg, Adenovirus receptors: Implications for tropism, treatment and targeting. Rev. Med. Virol. 19, 165-178 (2009).
36. K. Loré, W. C. Adams, M. J. Havenga, M. L. Precopio, L. Holterman, J. Goudsmit, R. A. Koup, Myeloid and plasmacytoid dendritic cells are susceptible to recombinant adenovirus vectors and stimulate polyfunctional memory T cell responses. J. Immunol. 179, 1721-1729 (2007).
37. + T-cell activation via CD46 ligation. Proc. Natl. Acad. Sci. U.S.A. 108, 7499-7504 (2011).
38. S. M. Todryk, M. Walther, P. Bejon, C. Hutchings, F. M. Thompson, B. C. Urban, D. W. Porter, A. V. Hill, Multiple functions of human T cells generated by experimental malaria challenge. Eur. J. Immunol. 39, 3042-3051 (2009).