Advances and future challenges in recombinant adenoviral vectored H5N1 influenza vaccines

Viruses

Volumn 4, Issue 11, 2012, Pages 2711-2735

  Zhang, Jianfeng ^a  

^a Vaxin Inc   (United States)

Author keywords

Cross protection; H5N1; Influenza vaccine; Pandemic influenza; Recombinant adenoviral vector

Indexed keywords

ADENOVIRUS VECTOR; ANTHRAX VACCINE; DNA VACCINE; INFLUENZA VACCINE;

ANTIBODY RESPONSE; CELLULAR IMMUNITY; CROSS PROTECTION; DRUG EFFICACY; DRUG SAFETY; HUMAN; HUMORAL IMMUNITY; IMMUNOGENICITY; INFECTION RISK; INFLUENZA A (H5N1); INFLUENZA VACCINATION; MASS IMMUNIZATION; NONHUMAN; REVIEW; RISK REDUCTION; SEROTYPE; TRANSGENE; VACCINE PRODUCTION; VIRAL CLEARANCE; VIRAL TROPISM; VIRUS IMMUNITY; VIRUS LIKE AGENT; VIRUS RECOMBINANT;

ADENOVIRIDAE; ADMINISTRATION, INTRANASAL; ANIMALS; GENETIC VECTORS; HUMANS; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA VACCINES; INFLUENZA, HUMAN; VACCINES, SYNTHETIC;

AVES; AVIAN INFLUENZA VIRUS; HUMAN ADENOVIRUS;

EID: 84870593766     PISSN: 19994915     EISSN: None     Source Type: Journal    
DOI: 10.3390/v4112711     Document Type: Review

References (178)

1. Thompson, W.W.; Shay, D.K.; Weintraub, E.; Brammer, L.; Bridges, C.B.; Cox, N.J.; Fukuda, K. Influenza-associated hospitalizations in the United States. JAMA 2004, 292, 1333-1340.
2. Centers for Disease Control and Prevention (CDC). Estimates of deaths associated with seasonal influenza: United States, 1976-2007. MMWR Morb. Mortal. Wkly. Rep. 2010, 59, 1057-1062.
3. Pérez Velasco, R.; Praditsitthikorn, N.; Wichmann, K.; Mohara, A.; Kotirum, S.; Tantivess, S.; Vallenas, C.; Harmanci, H.; Teerawattananon, Y. Systematic review of economic evaluations of preparedness strategies and interventions against influenza pandemics. PLoS One 2012, 7, e30333.
4. Lagacé-Wiens, P.R.; Rubinstein, E.; Gumel, A. Influenza epidemiology: Past, present, and future. Crit. Care Med. 2010, 38, e1-e9.
5. Fouchier, R.A.; Munster, V.; Wallensten, A.; Bestebroer, T.M.; Herfst, S.; Smith, D.; Rimmelzwaan, G.F.; Olsen, B.; Osterhaus, A.D. Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls. J. Virol. 2005, 79, 2814-2822.
6. Tong, S.; Li, Y.; Rivailler, P.; Conrardy, C.; Castillo, D.A.; Chen, L.M.; Recuenco, S.; Ellison, J.A.; Davis, C.T.; York, I.A.; Turmelle, A.S.; Moran, D.; Rogers, S.; Shi, M.; Tao, Y.; Weil, M.R.; Tang, K.; Rowe, L.A.; Sammons, S.; Xu, X.; Frace, M.; Lindblade, K.A.; Cox, N.J.; Anderson, L.J.; Rupprecht, C.E.; Donis, R.O. A distinct lineage of influenza A virus from bats. Proc. Natl. Acad. Sci. USA 2012, 109, 4269-4274.
7. Scholtissek, C.; Rohde, W.; Von Hoyningen, V.; Rott, R. On the origin of the human influenza virus subtypes H2N2 and H3N2. Virology 1978, 87, 13-20.
8. Reid, A.H.; Fanning, T.G.; Hultin, J.V.; Taubenberger, J.K. Origin and evolution of the 1918 "Spanish" influenza virus hemagglutinin gene. Proc. Natl. Acad. Sci. USA 1999, 96, 1651-1656.
9. Trifonov, V.; Khiabanian, H.; Rabadan, R. Geographic dependence, surveillance, and origins of the 2009 influenza A (H1N1) virus. N. Engl. J. Med. 2009, 361, 115-119.
10. World Health Organization (WHO). Antigenic and genetic characteristics of zoonotic influenza viruses and development of candidate vaccine viruses for pandemic preparedness. Wkly. Epidemiol. Rec. 2012, 87, 97-108.
11. Centers for Disease Control and Prevention (CDC). From the Centers for Disease Control and Prevention. Update: Isolation of avian influenza A(H5N1) viruses from humans: Hong Kong, 1997-1998. JAMA 1998, 279, 347-348.
12. Health Protection Agency. Influenza A virus subtype H5N1 infection in humans: Update. Commun. Dis. Rep. CDR Wkly. 1997, 7, 453.
13. Adams, S.; Sandrock, C. Avian influenza: Update. Med. Princ. Pract. 2010, 19, 421-432.
14. World Health Organization (WHO). 10 August 2012 update. Cumulative number of confirmed human cases for avian influenza A(H5N1) reported to WHO, 2003-2012. Available online: http://www.who.int/influenza/human_animal_interface/EN_GIP_20120502CumulativeNumberH5N1cases.pdf (accessed on 20 August 2012).
15. Dudley, J.P. Mammalian-transmissible highly pathogenic H5N1 influenza: Epidemiological context. MBio. 2012, 3, e00071-12.
16. Herfst, S.; Schrauwen, E.J.; Linster, M.; Chutinimitkul, S.; de Wit, E.; Munster, V.J.; Sorrell, E.M.; Bestebroer, T.M.; Burke, D.F.; Smith, D.J.; Rimmelzwaan, G.F.; Osterhaus, A.D.; Fouchier, R.A. Airborne transmission of influenza A/H5N1 virus between ferrets. Science 2012, 336, 1534-1541.
17. Imai, M.; Watanabe, T.; Hatta, M.; Das, S.C.; Ozawa, M.; Shinya, K.; Zhong, G.; Hanson, A.; Katsura, H.; Watanabe, S.; Li, C.; Kawakami, E.; Yamada, S.; Kiso, M.; Suzuki, Y.; Maher, E.A.; Neumann, G.; Kawaoka, Y. Experimental adaptation of an influenza H5 HA confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets. Nature 2012, 486, 420-428.
18. Russell, C.A.; Fonville, J.M.; Brown, A.E.; Burke, D.F.; Smith, D.L.; James, S.L.; Herfst, S.; van Boheemen, S.; Linster, M.; Schrauwen, E.J.; Katzelnick, L.; Mosterín, A.; Kuiken, T.; Maher, E.; Neumann, G.; Osterhaus, A.D.; Kawaoka, Y.; Fouchier, R.A.; Smith, D.J. The potential for respiratory droplet-transmissible A/H5N1 influenza virus to evolve in a mammalian host. Science 2012, 336, 1541-1547.
19. Webster, R.G. Mammalian-transmissible H5N1 influenza: the dilemma of dual-use research. MBio. 2012, 3, e00005-12.
20. World Health Organization (WHO). Pandemic influenza preparedness and response: A WHO guidance document. Availble online: http://whqlibdoc.who.int/publications/2009/9789241 547680_eng.pdf (accessed on 20 August 2012).
21. Lee, V.J.; Lye, D.C.; Wilder-Smith, A. Combination strategies for pandemic influenza response-A systematic review of mathematical modeling studies. BMC Med. 2009, 7, 76.
22. Schuchat, A.; Bell, B.P.; Redd, S.C. The science behind preparing and responding to pandemic influenza: the lessons and limits of science. Clin. Infect. Dis. 2011, 52, S8-12.
23. Emanuel, E.J.; Wertheimer, A. Public health. Who should get influenza vaccine when not all can? Science 2006, 312, 854-855.
24. Smith, K.A.; Colvin, C.J.; Weber, P.S.; Spatz, S.J.; Coussens, P.M. High titer growth of human and avian influenza viruses in an immortalized chick embryo cell line without the need for exogenous proteases. Vaccine 2008, 26, 3778-3782.
25. Rockman, S.; Brown, L. Pre-pandemic and pandemic influenza vaccines. Hum. Vaccin. 2010, 6, 792-801.
26. Clayville, L.R. Influenza update: A review of currently available vaccines. Pharmacy and Therapeutics 2011, 36, 659-684.
27. Centers for Disease Control and Prevention (CDC). Available online: http://www.cdc.gov/vaccines/pubs/vis/downloads/vis-flulive.pdf (accessed on 20 August 2012).
28. Haaheim, L.R.; Madhun, A.S.; Cox, R. Pandemic influenza vaccines-The challenges. Viruses 2009, 1, 1089-1109.
29. Singh, N.; Pandey, A.; Mittal, S.K. Avian influenza pandemic preparedness: Developing prepandemic and pandemic vaccines against a moving target. Expert Rev. Mol. Med. 2010, 12, e14.
30. Horimoto, T.; Kawaoka, Y. Designing vaccines for pandemic influenza. Curr. Top. Microbiol. Immunol. 2009, 333, 165-176.
31. Tutykhina, I.L.; Logunov, D.Y.; Shcherbinin, D.N.; Shmarov, M.M.; Tukhvatulin, A.I.; Naroditsky, B.S.; Gintsburg, A.L. Development of adenoviral vector-based mucosal vaccine against influenza. J. Mol. Med. (Berl). 2011, 89, 331-341.
32. Tang, D.C.; Zhang, J.; Toro, H.; Shi, Z.; Van Kampen, K.R. Adenovirus as a carrier for the development of influenza virus-free avian influenza vaccines. Expert Rev. Vaccines. 2009, 8, 469-481.
33. Vemula, S.V.; Mittal, S.K. Production of adenovirus vectors and their use as a delivery system for influenza vaccines. Expert. Opin. Biol. Ther. 2010, 10, 1469-1487.
34. Toro, H.; Tang, D.C. Protection of chickens against avian influenza with nonreplicating adenovirus-vectored vaccine. Poult. Sci. 2009, 88, 867-871.
35. Lambe, T. Novel viral vectored vaccines for the prevention of influenza. Mol. Med. 2012, doi: 10.2119/molmed.2012.00147.
36. Rowe, W.P.; Huebner, R.J.; Gilmore, L.K.; Parrott, R.H.; Ward, T.G. Isolation of a cytopathogenic agent from human adenoids undergoing spontaneous degeneration in tissue culture. Proc. Soc. Exp. Biol. Med. 1953, 84, 570-573.
37. Bangari, D.S.; Mittal, S.K. Development of nonhuman adenoviruses as vaccine vectors. Vaccine. 2006, 24, 849-862.
38. Smith, J.G.; Wiethoff, C.M.; Stewart, P.L.; Nemerow, G.R. Adenovirus. Curr. Top. Microbiol. Immunol. 2010, 343, 195-224.
39. Lichtenstein, D.L.; Wold, W.S. Experimental infections of humans with wild-type adenoviruses and with replication-competent adenovirus vectors: replication, safety, and transmission. Cancer Gene Ther. 2004, 11, 819-829.
40. Reddy, V.S.; Natchiar, S.K.; Stewart, P.L.; Nemerow, G.R. Crystal structure of human adenovirus at 3.5 A resolution. Science 2010, 329, 1071-1075.
41. Ginsberg, H.S. The life and times of adenoviruses. Adv. Virus. Res. 1999, 54, 1-13.
42. Russell, W.C. Adenoviruses: Update on structure and function. J. Gen. Virol. 2009, 90, 1-20.
43. Young, C.S. The structure and function of the adenovirus major late promoter. Curr. Top. Microbiol. Immunol. 2003, 272, 213-249.
44. Graham, F.L.; Smiley, J.; Russell, W.C.; Nairn, R. Characteristics of a human cell line transformed by DNA from human adenovirus type 5. J. Gen. Virol. 1977, 36, 59-74.
45. Kovesdi, I.; Hedley, S.J. Adenoviral producer cells. Viruses 2010, 2, 1681-1703.
46. Evans, R. K; Nawrocki, D.K.; Isopi, L.A.; Williams, D.M.; Casimiro, D.R.; Chin, S.; Chen, M.; Zhu, D.M.; Shiver, J.W.; Volkin, D.B. Development of stable liquid formulations for adenovirus-based vaccines. J. Pharm. Sci. 2004, 93, 2458-2475.
47. Croyle, M.A.; Cheng, X.; Wilson, J.M. Development of formulations that enhance physical stability of viral vectors for gene therapy. Gene. Ther. 2001, 8, 1281-1290.
48. Alcock, R.; Cottingham, M.G.; Rollier, C.S.; Furze, J.; De Costa, S.D.; Hanlon, M.; Spencer, A.J.; Honeycutt, J.D.; Wyllie, D.H.; Gilbert, S.C.; Bregu, M.; Hill, A.V. Long-term thermostabilization of live poxviral and adenoviral vaccine vectors at supraphysiological temperatures in carbohydrate glass. Sci. Transl. Med. 2010, 2, 19ra12.
49. Lewis, D.J.; Huo, Z.; Barnett, S.; Kromann, I.; Giemza, R.; Galiza, E.; Woodrow, M.; Thierry-Carstensen, B.; Andersen, P.; Novicki, D.; Del Giudice, G.; Rappuoli, R. Transient facial nerve paralysis (Bell's palsy) following intranasal delivery of a genetically detoxified mutant of Escherichia coli heat labile toxin. PLoS One 2009, 4, e6999.
50. Molinier-Frenkel, V.; Lengagne, R.; Gaden, F.; Hong, S.S.; Choppin, J.; Gahery-Ségard, H.; Boulanger, P.; Guillet, J.G. Adenovirus hexon protein is a potent adjuvant for activation of a cellular immune response. J. Virol. 2002, 76, 127-135.
51. Hartman, Z.C.; Appledorn, D.M.; Amalfitano, A. Adenovirus vector induced innate immune responses: Impact upon efficacy and toxicity in gene therapy and vaccine applications. Virus Res. 2008, 132, 1-14.
52. Wei, C.J.; Boyington, J.C.; McTamney, P.M.; Kong, W.P.; Pearce, M.B.; Xu, L.; Andersen, H.; Rao, S.; Tumpey, T.M.; Yang, Z.Y.; Nabel, G.J. Induction of broadly neutralizing H1N1 influenza antibodies by vaccination. Science 2010, 329, 1060-1064.
53. Van Kampen, K.R.; Shi, Z.; Gao, P.; Zhang, J.; Foster, K.W.; Chen, D.T.; Marks, D.; Elmets, C.A.; Tang, D.C. Safety and immunogenicity of adenovirus-vectored nasal and epicutaneous influenza vaccines in humans. Vaccine 2005, 23, 1029-1036.
54. Hashem, A.; Jaentschke, B.; Gravel, C.; Tocchi, M.; Doyle, T.; Rosu-Myles, M.; He, R.; Li, X. Subcutaneous immunization with recombinant adenovirus expressing influenza A nucleoprotein protects mice against lethal viral challenge. Hum. Vaccin. Immunother. 2012, 8, 425-430.
55. Song, K.; Bolton, D.L.; Wei, C.J.; Wilson, R.L.; Camp, J.V.; Bao, S.; Mattapallil, J.J.; Herzenberg, L.A.; Herzenberg, L.A.; Andrews, C.A.; Sadoff, J.C.; Goudsmit, J.; Pau, M.G.; Seder, R.A.; Kozlowski, P.A.; Nabel, G.J.; Roederer, M.; Rao, S.S. Genetic immunization in the lung induces potent local and systemic immune responses. Proc. Natl. Acad. Sci. USA 2010, 107, 22213-22218.
56. Roy, C.J.; Ault, A.; Sivasubramani, S.K.; Gorres, J.P.; Wei, C.J.; Andersen, H.; Gall, J.; Roederer, M.; Rao, S.S. Aerosolized adenovirus-vectored vaccine as an alternative vaccine delivery method. Respir. Res. 2011, 12, 153.
57. Saito, I.; Oya, Y.; Yamamoto, K.; Yuasa, T.; Shimojo, H. Construction of nondefective adenovirus type 5 bearing a 2.8-kilobase hepatitis B virus DNA near the right end of its genome. J. Virol. 1985, 54, 711-719.
58. Morin, J.E.; Lubeck, M.D.; Barton, J.E.; Conley, A.J.; Davis, A.R.; Hung, P.P. Recombinant adenovirus induces antibody response to hepatitis B virus surface antigen in hamsters. Proc. Natl. Acad. Sci. USA 1987, 84, 4626-4630.
59. Alkhatib, G.; Briedis, D.J. High-level eucaryotic in vivo expression of biologically active measles virus hemagglutinin by using an adenovirus type 5 helper-free vector system. J. Virol. 1988, 62, 2718-2727.
60. Eloit, M.; Gilardi-Hebenstreit, P.; Toma, B.; Perricaudet, M. Construction of a defective adenovirus vector expressing the pseudorabies virus glycoprotein gp50 and its use as a live vaccine. J. Gen. Virol. 1990, 71, 2425-2431.
61. Zhu, J.; Grace, M.; Casale, J.; Chang, A.T.; Musco, M.L.; Bordens, R.; Greenberg, R.; Schaefer, E.; Indelicato, S.R. Characterization of replication-competent adenovirus isolates from large-scale production of a recombinant adenoviral vector. Hum. Gene. Ther. 1999, 10, 113-121.
62. Lochmüller, H.; Jani, A.; Huard, J.; Prescott, S.; Simoneau, M.; Massie, B.; Karpati, G.; Acsadi, G. Emergence of early region 1-containing replication-competent adenovirus in stocks of replication-defective adenovirus recombinants (delta E1 + delta E3) during multiple passages in 293 cells. Hum. Gene. Ther. 1994, 5, 1485-1491.
63. Hermens, W.T.; Verhaagen, J. Adenoviral vector-mediated gene expression in the nervous system of immunocompetent Wistar and T cell-deficient nude rats: preferential survival of transduced astroglial cells in nude rats. Hum. Gene. Ther. 1997, 8, 1049-1063.
64. Fallaux, F.J.; Bout, A.; van der Velde, I.; van den Wollenberg, D.J.; Hehir, K.M.; Keegan, J.; Auger, C.; Cramer, S.J.; van Ormondt, H.; van der Eb, A.J.; Valerio, D.; Hoeben, R.C. New helper cells and matched early region 1-deleted adenovirus vectors prevent generation of replication-competent adenoviruses. Hum. Gene. Ther. 1998, 9, 1909-1917.
65. Ledwith, B.J.; Lanning, C.L.; Gumprecht, L. A; Anderson, C.A.; Coleman, J.B.; Gatto, N.T.; Balasubramanian, G.; Farris, G.M.; Kemp, R.K.; Harper, L.B.; Barnum, A.B.; Pacchione, S.J.; Mauer, K.L.; Troilo, P.F.; Brown, E.R.; Wolf, J.J.; Lebronl, J.A.; Lewis, J.A.; Nichols, W.W. Tumorigenicity assessments of Per. C6 cells and of an Ad5-vectored HIV-1 vaccine produced on this continuous cell line. Dev. Biol. (Basel) 2006, 123, 251-263; discussion 265-266.
66. Lusky, M. Good manufacturing practice production of adenoviral vectors for clinical trials. Hum Gene Ther. 2005, 16, 281-291.
67. Subramanian, S.; Kim, J.J.; Harding, F.; Altaras, G.M.; Aunins, J.G.; Zhou, W. Scaleable production of adenoviral vectors by transfection of adherent PER. C6 cells. Biotechnol. Prog. 2007, 23, 1210-1217.
68. Wang, Q.; Jia, X.C.; Finer, M.H. A packaging cell line for propagation of recombinant adenovirus vectors containing two lethal gene-region deletions. Gene. Ther. 1995, 2, 775-783.
69. Amalfitano, A.; Begy, C.R.; Chamberlain, J.S. Improved adenovirus packaging cell lines to support the growth of replication-defective gene-delivery vectors. Proc. Natl. Acad. Sci. USA 1996, 93, 3352-3356.
70. Gorziglia, M.I.; Kadan, M.J.; Yei, S.; Lim, J.; Lee, G.M.; Luthra, R.; Trapnell, B.C. Elimination of both E1 and E2 from adenovirus vectors further improves prospects for in vivo human gene therapy. J. Virol. 1996, 70, 4173-4178.
71. Gorziglia, M.I.; Lapcevich, C.; Roy, S.; Kang, Q.; Kadan, M.; Wu, V.; Pechan, P.; Kaleko, M. Generation of an adenovirus vector lacking E1, e2a, E3, and all of E4 except open reading frame 3. J. Virol. 1999, 73, 6048-6055.
72. Mitani, K.; Graham, F.L.; Caskey, C.T.; Kochanek, S. Rescue, propagation, and partial purification of a helper virus-dependent adenovirus vector. Proc. Natl. Acad. Sci. USA 1995, 92, 3854-3858.
73. Osada, T.; Yang, X.Y.; Hartman, Z.C.; Glass, O.; Hodges, B.L.; Niedzwiecki, D.; Morse, M.A.; Lyerly, H.K.; Amalfitano, A.; Clay, T.M. Optimization of vaccine responses with an E1, E2b and E3-deleted Ad5 vector circumvents pre-existing anti-vector immunity. Cancer Gene. Ther. 2009, 16, 673-682.
74. Weaver, E.A.; Nehete, P.N.; Buchl, S.S.; Senac, J.S.; Palmer, D.; Ng, P.; Sastry, K.J.; Barry, M.A. Comparison of replication-competent, first generation, and helper-dependent adenoviral vaccines. PLoS One 2009, 4, e5059.
75. Mast, T.C.; Kierstead, L.; Gupta, S.B.; Nikas, A.A.; Kallas, E.G.; Novitsky, V.; Mbewe, B.; Pitisuttithum, P.; Schechter, M.; Vardas, E.; Wolfe, N.D.; Aste-Amezaga, M.; Casimiro, D.R.; Coplan, P.; Straus, W.L.; Shiver, J.W. International epidemiology of human pre-existing adenovirus (Ad) type-5, type-6, type-26 and type-36 neutralizing antibodies: correlates of high Ad5 titers and implications for potential HIV vaccine trials. Vaccine 2010, 28, 950-957.
76. 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. International seroepidemiology of adenovirus serotypes 5, 26, 35, and 48 in pediatric and adult populations. Vaccine 2011, 29, 5203-5209.
77. Barouch, D.H.; McKay, P.F.; Sumida, S.M.; Santra, S.; Jackson, S.S.; Gorgone, D.A.; Lifton, M.A.; Chakrabarti, B.K.; Xu, L.; Nabel, G.J.; Letvin, N.L. Plasmid chemokines and colony-stimulating factors enhance the immunogenicity of DNA priming-viral vector boosting human immunodeficiency virus type 1 vaccines. J. Virol. 2003, 77, 8729-8735.
78. Pichla-Gollon, S.L.; Lin, S.W.; Hensley, S.E.; Lasaro, M.O.; Herkenhoff-Haut, L.; Drinker, M.; Tatsis, N.; Gao, G.P.; Wilson, J.M.; Ertl, H.C.; Bergelson, J.M. Effect of preexisting immunity on an adenovirus vaccine vector: in vitro neutralization assays fail to predict inhibition by antiviral antibody in vivo. J. Virol. 2009, 83, 5567-5573.
79. Yang, Z.Y.; Wyatt, L.S.; Kong, W.P.; Moodie, Z.; Moss, B.; Nabel, G.J. Overcoming immunity to a viral vaccine by DNA priming before vector boosting. J. Virol. 2003, 77, 799-803.
80. Vogels, R.; Zuijdgeest, D.; van Rijnsoever, R.; Hartkoorn, E.; Damen, I.; de Béthune, M.P.; Kostense, S.; Penders, G.; Helmus, N.; Koudstaal, W.; Cecchini, M.; Wetterwald, A.; Sprangers, M.; Lemckert, A.; Ophorst, O.; Koel, B.; van Meerendonk, M.; Quax, P.; Panitti, L.; Grimbergen, J.; Bout, A.; Goudsmit, J.; Havenga, M. Replication-deficient human adenovirus type 35 vectors for gene transfer and vaccination: Efficient human cell infection and bypass of preexisting adenovirus immunity. J. Virol. 2003, 77, 8263-8271.
81. Holterman, L.; Vogels, R.; van der Vlugt, R.; Sieuwerts, M.; Grimbergen, J.; Kaspers, J.; Geelen, E.; van der Helm, E.; Lemckert, A.; Gillissen, G.; Verhaagh, S.; Custers, J.; Zuijdgeest, D.; Berkhout, B.; Bakker, M.; Quax, P.; Goudsmit, J.; Havenga, M. 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. 2004, 78, 13207-13215.
82. Lemckert, A.A.; Grimbergen, J.; Smits, S.; Hartkoorn, E.; Holterman, L.; Berkhout, B.; Barouch, D.H.; Vogels, R.; Quax, P.; Goudsmit, J.; Havenga, M.J. Generation of a novel replication-incompetent adenoviral vector derived from human adenovirus type 49: manufacture on PER. C6 cells, tropism and immunogenicity. J. Gen. Virol. 2006, 87, 2891-2899.
83. Abbink, P.; Lemckert, A.A.; Ewald, B.A.; Lynch, D.M.; Denholtz, M.; Smits, S.; Holterman, L.; Damen, I.; Vogels, R.; Thorner, A.R.; O'Brien, K.L.; Carville, A.; Mansfield, K.G.; Goudsmit, J.; Havenga, M.J.; Barouch, D.H. Comparative seroprevalence and immunogenicity of six rare serotype recombinant adenovirus vaccine vectors from subgroups B and D. J. Virol. 2007, 81, 4654-4663.
84. Kahl, C.A.; Bonnell, J.; Hiriyanna, S.; Fultz, M.; Nyberg-Hoffman, C.; Chen, P.; King, C.R.; Gall, J.G. Potent immune responses and in vitro pro-inflammatory cytokine suppression by a novel adenovirus vaccine vector based on rare human serotype 28. Vaccine 2010, 28, 5691-5702.
85. Tatsis, N.; Tesema, L.; Robinson, E.R.; Giles-Davis, W.; McCoy, K.; Gao, G.P.; Wilson, J.M.; Ertl, H.C. Chimpanzee-origin adenovirus vectors as vaccine carriers. Gene. Ther. 2006, 13, 421-429.
86. Xiang, Z.; Gao, G.; Reyes-Sandoval, A.; Cohen, C.J.; Li, Y.; Bergelson, J.M.; Wilson, J.M.; Ertl, H.C. Novel, chimpanzee serotype 68-based adenoviral vaccine carrier for induction of antibodies to a transgene product. J. Virol. 2002, 76, 2667-2675.
87. Roy, S.; Kobinger, G.P.; Lin, J.; Figueredo, J.; Calcedo, R.; Kobasa, D.; Wilson, J.M. Partial protection against H5N1 influenza in mice with a single dose of a chimpanzee adenovirus vector expressing nucleoprotein. Vaccine 2007, 25, 6845-6851.
88. Singh, N.; Pandey, A.; Jayashankar, L.; Mittal, S.K. Bovine adenoviral vector-based H5N1 influenza vaccine overcomes exceptionally high levels of pre-existing immunity against human adenovirus. Mol. Ther. 2008, 16, 965-971.
89. Gao, Y.W.; Xia, X.Z.; Wang, L.G.; Liu, D.; Huang, G. Construction and experimental immunity of recombinant replication-competent canine adenovirus type 2 expressing hemagglutinin gene of H5N1 subtype tiger influenza virus. Wei Sheng Wu Xue Bao 2006, 46, 297-300.
90. Patel, A.; Tikoo, S.; Kobinger, G. A porcine adenovirus with low human seroprevalence is a promising alternative vaccine vector to human adenovirus 5 in an H5N1 virus disease model. PLoS One 2010, 5, e15301.
91. Wang, L.; Cheng, C.; Ko, S.Y.; Kong, W.P.; Kanekiyo, M.; Einfeld, D.; Schwartz, R.M.; King, C.R.; Gall, J.G.; Nabel, G.J. Delivery of human immunodeficiency virus vaccine vectors to the intestine induces enhanced mucosal cellular immunity. J. Virol. 2009, 83, 7166-7175.
92. 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. Adenovirus-based vaccines: Comparison of vectors from three species of adenoviridae. J. Virol. 2010, 84, 10522-10532.
93. Fitzgerald, J.C.; Gao, G.P.; Reyes-Sandoval, A.; Pavlakis, G.N.; Xiang, Z.Q.; Wlazlo, A.P.; Giles-Davis, W.; Wilson, J.M.; Ertl, H.C. A simian replication-defective adenoviral recombinant vaccine to HIV-1 gag. J. Immunol. 2003, 170, 1416-1422.
94. Frahm, N.; DeCamp, A.C.; Friedrich, D.P.; Carter, D.K.; Defawe, O.D.; Kublin, J.G.; Casimiro, D.R.; Duerr, A.; Robertson, M.N.; Buchbinder, S.P.; Huang, Y.; Spies, G.A.; De Rosa, S.C.; McElrath, M.J. Human adenovirus-specific T cells modulate HIV-specific T cell responses to an Ad5-vectored HIV-1 vaccine. J. Clin. Invest. 2012, 122, 359-367.
95. Seregin, S.S.; Amalfitano, A. Overcoming pre-existing adenovirus immunity by genetic engineering of adenovirus-based vectors. Expert Opin. Biol. Ther. 2009, 9, 1521-1531.
96. Dharmapuri, S.; Peruzzi, D.; Aurisicchio, L. Engineered adenovirus serotypes for overcoming anti-vector immunity. Expert Opin. Biol. Ther. 2009, 9, 1279-1287.
97. Stone, D.; Liu, Y.; Li, Z.Y.; Tuve, S.; Strauss, R.; Lieber, A. Comparison of adenoviruses from species B, C, E, and F after intravenous delivery. Mol. Ther. 2007, 15, 2146-2153.
98. Holst, P.J.; Ørskov, C.; Thomsen, A.R.; Christensen, J.P. 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. 2010, 184, 4431-4439.
99. Kaufman, D.R.; Bivas-Benita, M.; Simmons, N.L.; Miller, D.; Barouch, D.H. Route of adenovirus-based HIV-1 vaccine delivery impacts the phenotype and trafficking of vaccine-elicited CD8+ T lymphocytes. J. Virol. 2010, 84, 5986-5996.
100. Suda, T.; Kawano, M.; Nogi, Y.; Ohno, N.; Akatsuka, T.; Matsui, M. The route of immunization with adenoviral vaccine influences the recruitment of cytotoxic T lymphocytes in the lung that provide potent protection from influenza A virus. Antiviral Res. 2011, 91, 252-258.
101. Steitz, J.; Wagner, R.A.; Bristol, T.; Gao, W.; Donis, R.O.; Gambotto, A. Assessment of route of administration and dose escalation for an adenovirus-based influenza A Virus (H5N1) vaccine in chickens. Clin. Vaccine. Immunol. 2010, 17, 1467-1472.
102. Holman, D.H.; Penn-Nicholson, A.; Wang, D.; Woraratanadharm, J.; Harr, M.K.; Luo, M.; Maher, E.M.; Holbrook, M.R.; Dong, J.Y. A complex adenovirus-vectored vaccine against Rift Valley fever virus protects mice against lethal infection in the presence of preexisting vector immunity. Clin. Vaccine Immunol. 2009, 16, 1624-1632.
103. Appledorn, D.M.; Aldhamen, Y.A.; Godbehere, S.; Seregin, S.S.; Amalfitano, A. Sublingual administration of an adenovirus serotype 5 (Ad5)-based vaccine confirms Toll-like receptor agonist activity in the oral cavity and elicits improved mucosal and systemic cell-mediated responses against HIV antigens despite preexisting Ad5 immunity. Clin. Vaccine Immunol. 2011, 18, 150-160.
104. Xiang, Z.Q.; Gao, G.P.; Reyes-Sandoval, A.; Li, Y.; Wilson, J.M.; Ertl, H.C. Oral vaccination of mice with adenoviral vectors is not impaired by preexisting immunity to the vaccine carrier. J. Virol. 2003, 77, 10780-10789.
105. Pandey, A.; Singh, N.; Vemula, S.V.; Couëtil, L.; Katz, J.M.; Donis, R.; Sambhara, S.; Mittal, S.K. Impact of preexisting adenovirus vector immunity on immunogenicity and protection conferred with an adenovirus-based H5N1 influenza vaccine. PLoS One 2012, 7, e33428.
106. Xiang, Z.Q.; Yang, Y.; Wilson, J.M.; Ertl, H.C. A replication-defective human adenovirus recombinant serves as a highly efficacious vaccine carrier. Virology 1996, 219, 220-227.
107. Shi, Z.; Zeng, M.; Yang, G.; Siegel, F.; Cain, L.J.; van Kampen, K.R.; Elmets, C.A.; Tang, D.C. Protection against tetanus by needle-free inoculation of adenovirus-vectored nasal and epicutaneous vaccines. J. Virol. 2001, 75, 11474-11482.
108. Yu, J.R.; Kim, S.; Lee, J.B.; Chang, J. Single intranasal immunization with recombinant adenovirus-based vaccine induces protective immunity against respiratory syncytial virus infection. J. Virol. 2008, 82, 2350-2357.
109. Croyle, M.A.; Patel, A.; Tran, K.N.; Gray, M.; Zhang, Y.; Strong, J.E.; Feldmann, H.; Kobinger, G.P. Nasal delivery of an adenovirus-based vaccine bypasses pre-existing immunity to the vaccine carrier and improves the immune response in mice. PLoS One 2008, 3, e3548.
110. Xu, Q.; Pichichero, M.E.; Simpson, L.L.; Elias, M.; Smith, L.A.; Zeng, M. An adenoviral vector-based mucosal vaccine is effective in protection against botulism. Gene Ther. 2009, 16, 367-375.
111. Richardson, J.S.; Abou, M.C.; Tran, K.N.; Kumar, A.; Sahai, B.M.; Kobinger, G.P. Impact of systemic or mucosal immunity to adenovirus on Ad-based Ebola virus vaccine efficacy in guinea pigs. J. Infect. Dis. 2011, 204, S1032-S1042.
112. Draghia, R.; Caillaud, C.; Manicom, R.; Pavirani, A.; Kahn, A.; Poenaru, L. Gene delivery into the central nervous system by nasal instillation in rats. Gene Ther. 1995, 2, 418-423.
113. Damjanovic, D.; Zhang, X.; Mu, J.; Medina, M.F.; Xing, Z. Organ distribution of transgene expression following intranasal mucosal delivery of recombinant replication-defective adenovirus gene transfer vector. Genet. Vaccines Ther. 2008, 6, 5.
114. Huang, D.; Pereboev, A.V.; Korokhov, N.; He, R.; Larocque, L.; Gravel, C.; Jaentschke, B.; Tocchi, M.; Casley, W.L.; Lemieux, M.; Curiel, D.T.; Chen, W.; Li, X. Significant alterations of biodistribution and immune responses in Balb/c mice administered with adenovirus targeted to CD40(+) cells. Gene Ther. 2008, 15, 298-308.
115. Lemiale, F.; Kong, W.P.; Akyürek, L.M.; Ling, X.; Huang, Y.; Chakrabarti, B.K.; Eckhaus, M.; Nabel, G.J. Enhanced mucosal immunoglobulin A response of intranasal adenoviral vector human immunodeficiency virus vaccine and localization in the central nervous system. J. Virol. 2003, 77, 10078-10087.
116. Näslund, T.I.; Uyttenhove, C.; Nordström, E.K.; Colau, D.; Warnier, G.; Jondal, M.; Van den Eynde, B.J.; Liljeström, P. Comparative prime-boost vaccinations using Semliki Forest virus, adenovirus, and ALVAC vectors demonstrate differences in the generation of a protective central memory CTL response against the P815 tumor. J. Immunol. 2007, 178, 6761-6769.
117. Barefoot, B.; Thornburg, N.J.; Barouch, D.H.; Yu, J.S.; Sample, C.; Johnston, R.E.; Liao, H.X.; Kepler, T.B.; Haynes, B.F.; Ramsburg, E. Comparison of multiple vaccine vectors in a single heterologous prime-boost trial. Vaccine 2008, 26, 6108-6118.
118. Gao, W.; Soloff, A.C.; Lu, X.; Montecalvo, A.; Nguyen, D.C.; Matsuoka, Y.; Robbins, P.D.; Swayne, D.E.; Donis, R.O.; Katz, J.M.; Barratt-Boyes, S.M.; Gambotto, A. Protection of mice and poultry from lethal H5N1 avian influenza virus through adenovirus-based immunization. J. Virol. 2006, 80, 1859-1864.
119. Hoelscher, M.A.; Garg, S.; Bangari, D.S.; Belser, J.A.; Lu, X.; Stephenson, I.; Bright, R.A.; Katz, J.M.; Mittal, S.K.; Sambhara, S. Development of adenoviral-vector-based pandemic influenza vaccine against antigenically distinct human H5N1 strains in mice. Lancet 2006, 367, 475-481.
120. Thomas, P.G.; Keating, R.; Hulse-Post, D.J.; Doherty, P.C. Cell-mediated protection in influenza infection. Emerg. Infect. Dis. 2006, 12, 48-54.
121. Lin, J.; Somanathan, S.; Roy., S.; Calcedo, R.; Wilson, J.M. Lung homing CTLs and their proliferation ability are important correlates of vaccine protection against influenza. Vaccine 2010, 28, 5669-5675.
122. Toro, H.; Tang, D.C.; Suarez, D.L.; Zhang, J.; Shi, Z. Protection of chickens against avian influenza with non-replicating adenovirus-vectored vaccine. Vaccine 2008, 26, 2640-2646.
123. Shmarov, M.M.; Sedova, E.S.; Verkhovskaya, L.V.; Rudneva, I.A.; Bogacheva, E.A.; Barykova, Y.A.; Shcherbinin, D.N.; Lysenko, A.A.; Tutykhina, I.L.; Logunov, D.Y.; Smirnov, Y.A.; Naroditsky, B.S.; Gintsburg, A.L. Induction of a protective heterosubtypic immune response against the Influenza virus by using recombinant adenoviral vectors expressing hemagglutinin of the Influenza H5 virus. Acta Naturae 2010, 2, 111-118.
124. Du, L.; Zhou, Y.; Jiang, S. Research and development of universal influenza vaccines. Microbes Infect. 2010, 12, 280-286.
125. Toro, H., Tang, D.C.; Suarez, D.L.; Sylte, M.J.; Pfeiffer, J.; Van Kampen, K.R. Protective avian influenza in ovo vaccination with non-replicating human adenovirus vector. Vaccine 2007, 25, 2886-2891.
126. Soboleski, M.R.; Gabbard, J.D.; Price, G.E.; Misplon, J.A.; Lo, C.Y.; Perez, D.R.; Ye, J.; Tompkins, S.M.; Epstein, S.L. Cold-adapted influenza and recombinant adenovirus vaccines induce cross-protective immunity against pH1N1 challenge in mice. PLoS One 2011, 6, e21937.
127. Price, G.E.; Soboleski, M.R.; Lo, C.Y.; Misplon, J.A.; Quirion, M.R.; Houser, K.V.; Pearce, M.B.; Pappas, C.; Tumpey, T.M.; Epstein, S.L. Single-dose mucosal immunization with a candidate universal influenza vaccine provides rapid protection from virulent H5N1, H3N2 and H1N1 viruses. PLoS One 2010, 5, e13162.
128. Park, K.S.; Lee, J.; Ahn, S.S.; Byun, Y.H.; Seong, B.L.; Baek, Y.H.; Song, M.S.; Choi, Y.K.; Na, Y.J.; Hwang, I.; Sung, Y.C.; Lee, C.G. Mucosal immunity induced by adenovirus-based H5N1 HPAI vaccine confers protection against a lethal H5N2 avian influenza virus challenge. Virology 2009, 395, 182-189.
129. Price, G.E.; Soboleski, M.R.; Lo, C.Y.; Misplon, J.A.; Pappas, C.; Houser, K.V.; Tumpey, T.M.; Epstein, S.L. Vaccination focusing immunity on conserved antigens protects mice and ferrets against virulent H1N1 and H5N1 influenza A viruses. Vaccine 2009, 27, 6512-6521.
130. Hasegawa, H.; Ichinohe, T.; Ainai, A.; Tamura, S.; Kurata, T. Development of mucosal adjuvants for intranasal vaccine for H5N1 influenza viruses. Ther. Clin. Risk Manag. 2009, 5, 125-132.
131. Tamura, S.; Tanimoto, T.; Kurata, T. Mechanisms of broad cross-protection provided by influenza virus infection and their application to vaccines. Jpn. J. Infect. Dis. 2005, 58, 195-207.
132. Ichinohe, T.; Tamura, S.; Kawaguchi, A.; Ninomiya, A.; Imai, M.; Itamura, S.; Odagiri, T.; Tashiro, M.; Takahashi, H.; Sawa, H.; Mitchell, W.M.; Strayer, D.R.; Carter, W.A.; Chiba, J.; Kurata, T.; Sata, T.; Hasegawa, H. Cross-protection against H5N1 influenza virus infection is afforded by intranasal inoculation with seasonal trivalent inactivated influenza vaccine. J. Infect. Dis. 2007, 196, 1313-1320.
133. Perrone, L.A.; Ahmad, A.; Veguilla, V.; Lu, X.; Smith, G.; Katz, J.M.; Pushko, P.; Tumpey, T.M. Intranasal vaccination with 1918 influenza virus-like particles protects mice and ferrets from lethal 1918 and H5N1 influenza virus challenge. J. Virol. 2009, 83, 5726-5734.
134. Lau, Y.F.; Wright, A.R.; Subbarao, K. The contribution of systemic and pulmonary immune effectors to vaccine-induced protection from H5N1 influenza virus infection. J. Virol. 2012, 86, 5089-5098.
135. Gustin, K.M.; Maines, T.R.; Belser, J.A.; van Hoeven, N.; Lu, X.; Dong, L.; Isakova-Sivak, I.; Chen, L.M.; Voeten, J.T.; Heldens, J.G.; van den Bosch, H.; Cox, N.J.; Tumpey, T.M.; Klimov, A.I.; Rudenko, L.; Donis, R.O.; Katz, J.M. Comparative immunogenicity and cross-clade protective efficacy of mammalian cell-grown inactivated and live attenuated H5N1 reassortant vaccines in ferrets. J. Infect. Dis. 2011, 204, 1491-1499.
136. Zhang, J.; Tarbet, E.B.; Feng, T.; Shi, Z.; Van Kampen, K.R.; Tang, D.C. Adenovirus-vectored drug-vaccine duo as a rapid-response tool for conferring seamless protection against influenza. PLoS One 2011, 6, e22605.
137. McConnell, M.J.; Hanna, P.C.; Imperiale, M.J. Adenovirus-based prime-boost immunization for rapid vaccination against anthrax. Mol. Ther. 2007, 15, 203-210.
138. Holst, P.J.; Bartholdy, C.; Stryhn, A.; Thomsen, A.R.; Christensen, J.P. Rapid and sustained CD4(+) T-cell-independent immunity from adenovirus-encoded vaccine antigens. J. Gen. Virol. 2007, 88, 1708-1716.
139. Fernández, E.; Toledo, J.R.; Chiong, M.; Parra, F.; Rodríguez, E.; Montero, C.; Méndez, L.; Capucci, L.; Farnós, O. Single dose adenovirus vectored vaccine induces a potent and long-lasting immune response against rabbit hemorrhagic disease virus after parenteral or mucosal administration. Vet. Immunol. Immunopathol. 2011, 142, 179-188.
140. Weaver, E.A.; Rubrum, A.M.; Webby, R.J.; Barry, M.A. Protection against divergent influenza H1N1 virus by a centralized influenza hemagglutinin. PLoS One 2011, 6, e18314.
141. Hoelscher, M.A.; Jayashankar, L.; Garg, S.; Veguilla, V.; Lu, X.; Singh, N.; Katz, J.M.; Mittal, S.K.; Sambhara, S. New pre-pandemic influenza vaccines: an egg-and adjuvant-independent human adenoviral vector strategy induces long-lasting protective immune responses in mice. Clin. Pharmacol. Ther. 2007, 82, 665-671.
142. Rao, S.S.; Kong, W.P.; Wei, C.J.; Van Hoeven, N.; Gorres, J.P.; Nason, M.; Andersen, H.; Tumpey, T.M.; Nabel, G.J. Comparative efficacy of hemagglutinin, nucleoprotein, and matrix 2 protein gene-based vaccination against H5N1 influenza in mouse and ferret. PLoS One 2010, 5, e9812.
143. Patel, A.; Tran, K.; Gray, M.; Li, Y.; Ao, Z.; Yao, X.; Kobasa, D.; Kobinger, G.P. Evaluation of conserved and variable influenza antigens for immunization against different isolates of H5N1 viruses. Vaccine 2009, 27, 3083-3089.
144. Chen, Q.; Kuang, H.; Wang, H.; Fang, F.; Yang, Z.; Zhang, Z.; Zhang, X.; Chen, Z. Comparing the ability of a series of viral protein-expressing plasmid DNAs to protect against H5N1 influenza virus. Virus Gene. 2009, 38, 30-38.
145. Nayak, B.; Kumar, S.; DiNapoli, J.M.; Paldurai, A.; Perez, D.R.; Collins, P.L.; Samal, S.K. Contributions of the avian influenza virus HA, NA, and M2 surface proteins to the induction of neutralizing antibodies and protective immunity. J. Virol. 2010, 84, 2408-2420.
146. World Health Organisation (WHO); World Organisation for Animals Health United Nations (OIE); Food and Agriculture Organisation (FAO) H5N1 Evolution Working Group. Continued evolution of highly pathogenic avian influenza A (H5N1): updated nomenclature. Influenza Other Respi. Viruses 2012, 6, 1-5.
147. Hoelscher, M.A.; Singh, N.; Garg, S.; Jayashankar, L.; Veguilla, V.; Pandey, A.; Matsuoka, Y.; Katz, J.M.; Donis, R.; Mittal, S.K.; Sambhara, S. A broadly protective vaccine against globally dispersed clade 1 and clade 2 H5N1 influenza viruses. J. Infect. Dis. 2008, 197, 1185-1188.
148. Hu, X.; Meng, W.; Dong, Z.; Pan, W.; Sun, C.; Chen, L. Comparative immunogenicity of recombinant adenovirus-vectored vaccines expressing different forms of hemagglutinin (HA) proteins from the H5 serotype of influenza A viruses in mice. Virus Res. 2011, 155, 156-162.
149. Patel, A.; Gray, M.; Li, Y.; Kobasa, D.; Yao, X.; Kobinger, G.P. Co-administration of certain DNA vaccine combinations expressing different H5N1 influenza virus antigens can be beneficial or detrimental to immune protection. Vaccine 2012, 30, 626-636.
150. Holman, D.H.; Wang, D.; Raja, N.U.; Luo, M.; Moore, K.M.; Woraratanadharm, J.; Mytle, N.; Dong, J.Y. Multi-antigen vaccines based on complex adenovirus vectors induce protective immune responses against H5N1 avian influenza viruses. Vaccine 2008, 26, 2627-2639.
151. Pratt, W.D.; Wang, D.; Nichols, D.K.; Luo, M.; Woraratanadharm, J.; Dye, J.M.; Holman, D.H.; Dong, J.Y. Protection of nonhuman primates against two species of Ebola virus infection with a single complex adenovirus vector. Clin. Vaccine Immunol. 2010, 17, 572-581.
152. Holman, D.H.; Wang, D.; Raviprakash, K.; Raja, N.U.; Luo, M.; Zhang, J.; Porter, K, R.; Dong, J.Y. Two complex, adenovirus-based vaccines that together induce immune responses to all four dengue virus serotypes. Clin. Vaccine Immunol. 2007, 14, 182-189.
153. Epstein, S.L.; Kong, W.P.; Misplon, J.A.; Lo, C.Y.; Tumpey, T.M.; Xu, L.; Nabel, G.J. Protection against multiple influenza A subtypes by vaccination with highly conserved nucleoprotein. Vaccine 2005, 23, 5404-5410.
154. Tompkins, S., M.; Zhao, Z.S.; Lo, C.Y.; Misplon, J.A.; Liu, T.; Ye, Z.; Hogan, R.J.; Wu, Z.; Benton, K.A.; Tumpey, T.M.; Epstein, S.L. Matrix protein 2 vaccination and protection against influenza viruses, including subtype H5N1. Emerg. Infect. Dis. 2007, 13, 426-435.
155. Lo, C.Y.; Wu, Z.; Misplon, J.A.; Price, G.E.; Pappas, C.; Kong, W.P.; Tumpey, T.M.; Epstein, S.L. Comparison of vaccines for induction of heterosubtypic immunity to influenza A virus: cold-adapted vaccine versus DNA prime-adenovirus boost strategies. Vaccine 2008, 26, 2062-2072.
156. Jegerlehner, A.; Schmitz, N.; Storni, T.; Bachmann, M.F. Influenza A vaccine based on the extracellular domain of M2: Weak protection mediated via antibody-dependent NK cell activity. J. Immunol. 2004, 172, 5598-5605.
157. Wei, C.J.; Yassine, H.M.; McTamney, P.M.; Gall, J.G.; Whittle, J.R.; Boyington, J.C.; Nabel, G.J. Elicitation of broadly neutralizing influenza antibodies in animals with previous influenza exposure. Sci. Transl. Med. 2012, 4, 147ra114.
158. Maeda, K.; West, K.; Hayasaka, D.; Ennis, F.A.; Terajima, M. Recombinant adenovirus vector vaccine induces stronger cytotoxic T-cell responses than recombinant vaccinia virus vector, plasmid DNA, or a combination of these. Viral Immunol. 2005, 18, 657-667.
159. Lin, S.C.; Huang, M.H.; Tsou, P.C.; Huang, L.M.; Chong, P.; Wu, S.C. Recombinant trimeric HA protein immunogenicity of H5N1 avian influenza viruses and their combined use with inactivated or adenovirus vaccines. PLoS One 2011, 6, e20052.
160. Hung, P.P.; Chanda, P.K.; Natuk, R.J.; Mason, B.B.; Chengalvala, M.; Bhat, B.M.; Molnar-Kimber, K.L.; Dheer, S.K.; Morin, J.E.; Mizutani, S.; et al. Adenovirus vaccine strains genetically engineered to express HIV-1 or HBV antigens for use as live recombinant vaccines. Nat. Immun. Cell Growth Regul. 1990, 9, 160-164.
161. Hsu, K.H.; Lubeck, M.D.; Bhat, B.M.; Bhat, R.A.; Kostek, B.; Selling, B.H.; Mizutani, S.; Davis, A.R.; Hung, P.P. Efficacy of adenovirus-vectored respiratory syncytial virus vaccines in a new ferret model. Vaccine 1994, 12, 607-612.
162. Alexander, J.; Ward, S.; Mendy, J.; Manayani, D.J.; Farness, P.; Avanzini, J.B.; Guenther, B.; Garduno, F.; Jow, L.; Snarsky, V.; Ishioka, G.; Dong, X.; Vang, L.; Newman, M.J.; Mayall, T. Pre-clinical evaluation of a replication-competent recombinant adenovirus serotype 4 vaccine expressing influenza H5 hemagglutinin. PLoS One 2012, 7, e31177.
163. National Institutes of Health. Available online: http://www.clinicaltrials.gov/(accessed on 20 August 2012).
164. Gao, Y.W.; Xia, X.Z.; Wang, L.G.; Liu, D.; Huang, G. Construction and experimental immunity of recombinant replication-competent canine adenovirus type 2 expressing hemagglutinin gene of H5N1 subtype tiger influenza virus. Wei Sheng Wu Xue Bao 2006, 46, 297-300.
165. Pfeiffer, D.U.; Minh, P.Q.; Martin, V.; Epprecht, M.; Otte, M.J. An analysis of the spatial and temporal patterns of highly pathogenic avian influenza occurrence in Vietnam using national surveillance data. Vet. J. 2007, 174, 302-309.
166. Les, S.; Dung, D.H. Vaccination of poultry in Vietnam against H5N1 highly pathogenic avian influenza. Available online: http://www.aitoolkit.org/site/DefaultSite/filesystem/documents/CASE%20STUDY_07-09-09%20final.pdf (accessed on 20 August 2012).
167. Sánchez, Ramos O.; González, Pose A.; Gómez-Puerta, S.; Noda, Gomez J.; Vega Redondo, A.; Águila Benites, J.C.; Suárez Amarán, L.; Toledo, A.J.R. Avian CD154 enhances humoral and cellular immune responses induced by an adenovirus vector-based vaccine in chickens. Comp. Immunol. Microbiol. Infect. Dis. 2011, 34, 259-265.
168. Toro, H.; Suarez, D.L.; Tang, D.C.; van Ginkel, F.W.; Breedlovea, C. Avian influenza mucosal vaccination in chickens with replication-defective recombinant adenovirus vaccine. Avian. Dis. 2011, 55, 43-47.
169. Madore, D.V.; Meade, B.D.; Rubin, F.; Deal, C.; Lynn, F.; Meeting Contributors. Utilization of serologic assays to support efficacy of vaccines in nonclinical and clinical trials: meeting at the crossroads. Vaccine 2010, 28, 4539-4547.
170. Epstein, S.L.; Price, G.E. Cross-protective immunity to influenza A viruses. Expert Rev. Vaccines 2010, 9, 1325-1341.
171. Chen, M.W.; Cheng, T.J.; Huang, Y.; Jan, J.T.; Ma, S.H.; Yu, A.L.; Wong, C.H.; Ho, D.D. A consensus-hemagglutinin-based DNA vaccine that protects mice against divergent H5N1 influenza viruses. Proc. Natl. Acad. Sci. USA 2008, 105, 13538-13543.
172. Laddy, D.J.; Yan, J.; Kutzler, M.; Kobasa, D.; Kobinger, G.P.; Khan, A.S.; Greenhouse, J.; Sardesai, N.Y.; Draghia-Akli, R.; Weiner, D.B. Heterosubtypic protection against pathogenic human and avian influenza viruses via in vivo electroporation of synthetic consensus DNA antigens. PLoS One 2008, 3, e2517.
173. Jones, F.R.; Gabitzsch, E.S.; Xu, Y.; Balint, J.P.; Borisevich, V.; Smith, J.; Smith, J.; Peng, B.H.; Walker, A.; Salazar, M.; Paessler, S. Prevention of influenza virus shedding and protection from lethal H1N1 challenge using a consensus 2009 H1N1 HA and NA adenovirus vector vaccine. Vaccine 2011, 29, 7020-7026.
174. Steitz, J.; Barlow, P.G.; Hossain, J.; Kim, E.; Okada, K.; Kenniston, T.; Rea, S.; Donis, R.O.; Gambotto, A. A candidate H1N1 pandemic influenza vaccine elicits protective immunity in mice. PLoS One 2010, 5, e10492.
175. Catanzaro, A.T.; Koup, R.A.; Roederer, M.; Bailer, R.T.; Enama, M.E.; Moodie, Z.; Gu, L.; Martin, J.E.; Novik, L.; Chakrabarti, B.K.; Butman, B.T.; Gall, J.G.; King, C.R.; Andrews, C.A.; Sheets, R.; Gomez, P.L.; Mascola, J.R.; Nabel, G.J.; Graham, B.S.; Vaccine Research Center 006 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. 2006, 194, 1638-1649.
176. International Federation of Pharmaceutical Manufacturers & Associations. Cell culture based vaccines. Available online: http://www.ifpma.org/resources/influenza-vaccines/influenza-vaccines/cell-culture-based-vaccine.html (accessed on 21 October 2012).
177. Novartis Vaccines and Diagnostics, Inc. Novartis Holly Springs cell culture influenza vaccine manufacturing facility first to be declared pandemic ready by U.S. government. Available online: http://www.novartisvaccines.com/newsroom/media-releases/2011/Holly_Springs_HHS_pandemic_ready_US_Template_FINAL.pdf (accessed on 21 October 2012).
178. Girard M.P., Katz J.M., Pervikov Y., Hombach J., Tam J.S. Report of the 7th meeting on Evaluation of Pandemic Influenza Vaccines in Clinical Trials, World Health Organization, Geneva, 17-18, February 2011. Vaccine 2011, 29, 7579-7586.