WJV  Vol.3 No.3 , August 2013
Adenoviral Vectors in Veterinary Vaccine Development: Potential for Further Development
Abstract: Vaccines are an integral part of veterinary disease prevention. However there are still a significant number of veterinary diseases for which vaccines do not currently exist or where currently available vaccines do not provide adequate immunity. Adenoviruses have transitioned from tools for gene replacement therapy to bona fide vaccine delivery vehicles because of their ability to elicit potent cell-mediated and humoral responses making them ideal for use against viruses and other intracellular pathogens. Adenoviral vector based vaccines are likely to play a significant role in overcoming these problems in the future. However, this vector is under utilized in veterinary vaccine development at this time. This review focuses on adenoviral vector based vaccines developed to date and explores the potential for veterinary vaccine development based upon this platform: advantages and potential disadvantages of this technology are discussed as well as the potential for developing efficacious commercial veterinary adenoviral vector based vaccines.
Cite this paper: O. Ndi, M. Barton and T. Vanniasinkam, "Adenoviral Vectors in Veterinary Vaccine Development: Potential for Further Development," World Journal of Vaccines, Vol. 3 No. 3, 2013, pp. 111-121. doi: 10.4236/wjv.2013.33016.

[1]   P. Carnieli, A. M. Ventura and E. L. Durigon, “Construction of a Recombinant Plasmid pSH-G Containing the Rabies-Virus Glycoprotein G Gene,” Journal of Venomous Animals and Toxins including Tropical Diseases, Vol. 13, No. 4, 2007, pp. 874-880. doi:10.1590/S1678-91992007000400015

[2]   M. Lombard, P. P. Pastoret and A. M. Moulin, “A Brief History of Vaccines and Vaccination,” Revue et Scientifique Technique (International Office of Epizootics), Vol. 26, No. 1, 2007, pp. 29-48.

[3]   E. N. T. Meeusen, J. Walker, A. Peters, P. Pastoret and G. Jungersen, “Current Status of Veterinary Vaccines,” Clinical Microbiology Reviews, Vol. 20, No. 3, 2007, pp. 489-510. doi:10.1128/CMR.00005-07

[4]   D. J. Alexander, “Newcastle Disease,” In: H. G. Purchase, L. H. Arp, C. H. Domermuth and J. E. Pearson, Eds., A Laboratory Manual for the Isolation and Identification of Avian Pathogens, American Association for Avian Pathologists, Inc., Philadelphia, 1989, pp. 114-120.

[5]   A. Brun, E. Albina, T. Barret, D. A. G. Chapman, M. Czub, L. K. Dixon, G. M. Keil, B. Klonjkowski, M.-F. Le Potier, G. V. Libeau, J. Ortego, J. Richardson and H. H. Takamatsu, “Antigen Delivery Systems for Veterinary Vaccine Development: Viral-Vector Based Delivery Systems,” Vaccine, Vol. 26, No. 51, 2008, pp. 6508-6528. doi:10.1016/j.vaccine.2008.09.044

[6]   M. M. Erdmana, K. I. Kamrud, D. L. Harris and J. Smith, “Alphavirus Replicon Particle Vaccines Developed for Use in Humans Induce High Levels of Antibodies to Influenza Virus Hemagglutinin in Swine: Proof of Concept,” Vaccine, Vol. 28, No. 3, 2010, pp. 594-596. doi:10.1016/j.vaccine.2009.10.015

[7]   E. S. Gabitzsch, Y. Xu, L. H. Yoshida, J. Balint, A. Amalfitano and F. R. Jones, “Novel Adenovirus Type 5 Vaccine Platform Induces Cellular Immunity against HIV-1 Gag, Pol, Nef Despite the Presence of Ad5 Immunity,” Vaccine, Vol. 27, No. 46, 2009, pp. 6394-6398. doi:10.1016/j.vaccine.2009.06.028

[8]   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 and N. J. Sullivan, “Recombinant Adenovirus Serotype 26 (Ad26) and Ad35 Vaccine Vectors Bypass Immunity to Ad5 and Protect Nonhuman Primates against Ebolavirus Challenge,” Journal of Virology, Vol. 85, No. 9, 2011, pp. 4222-4233. doi:10.1128/JVI.02407-10

[9]   M. C. Pardo, J. E. Bauman and M. Mackowiak, “Protection of Dogs against Canine Distemper by Vaccination with a Canarypox Virus Recombinant Expressing Canine Distemper Virus Fusion and Hemoglutinin Glycoproteins,” American Journal of Veterinary Research, Vol. 58, No. 8, 1997, pp. 833-836.

[10]   D. Kuck, T. Lau, B. Leuchs, A. Kern, M. Müller, L. Gissmann and J. A. Kleinschmidt, “Intranasal Vaccination with Recombinant Adeno-Associated Virus Type 5 against Human Papillomavirus Type 16 L1,” Journal of Virology, Vol. 80, No. 6, 2006, pp. 2621-2630. doi:10.1128/JVI.80.6.2621-2630.2006

[11]   M. Benko, P. élo, K. Ursu, W. Ahne, S. E. LaPatra, D. Thomson and B. Harrach, “First Molecular Evidence for the Existence of Distinct Fish and Snake Adenoviruses,” Journal of Virology, Vol. 76, No. 19, 2002, pp. 10056-10059. doi:10.1128/JVI.76.19.10056-10059.2002

[12]   A. J. Davison, M. Benko and B. Harrach, “Genetic Content and Evolution of Adenoviruses,” Journal of General Virology, Vol. 84, No. 11, 2003, pp. 2895-2908. doi:10.1099/vir.0.19497-0

[13]   J. Dean, K. S. Latimer, J. L. Oaks, M. Schrenzel, P. T. Redig and A. Wunschman, “Falcon Adenovirus Infection in Breeding Taita Falcons (Falco fasciinucha),” Journal of Veterinary Diagnostic Investigation, Vol. 18, No. 3, 2006, pp. 282-286. doi:10.1177/104063870601800310

[14]   K. Erles, E. J. Dubovi, H. W. Brooks and J. Brownlie, “Longitudinal Study of Viruses Associated with Canine Infectious Respiratory Disease,” Journal of Clinical Microbiology, Vol. 42, No. 10, 2004, pp. 4524-4529. doi:10.1128/JCM.42.10.4524-4529.2004

[15]   R. P. Hedrick, J. Speas, M. L. Kent and T. McDowell, “Adenovirus Like Particles Associated with a Disease of Cultured White Sturgeon Acipenser transmontanus,” Canadian Journal of Fish and Aquatic Science, Vol. 42, No. 7, 1985, pp. 1231-1235. doi:10.1139/f85-165

[16]   E. R. Kovacs, J. Mate, D. Adam, H. Balazs and M. Benko, “Recognition and Partial Genome Characterization by Non-Specific DNA Amplification and PCR of a New Siadenovirus Species in a Sample Originating from Parus major, a Great Tit,” Journal of Virological Methods, Vol. 163, No. 2, 2010, pp. 262-268. doi:10.1016/j.jviromet.2009.10.007

[17]   T. H. Lim, B. Y. Kim, M. S. Kim, J. H. Jang, D. H. Lee, Y. K. Kwon, J. B Lee, S. Y. Park, I. S. Choi and C. S. Song, “Outbreak of Gizzard Erosion Associated with Fowl Adenovirus Infection in Korea,” Poultry Science, Vol. 91, No. 5, 2012, pp. 1113-1117. doi:10.3382/ps.2011-02050

[18]   H. D. Lehmkuhl and R. C. Cutlip, “A New Goat Adenovirus Isolate Proposed as the Prototype Strain for Goat Adenovirus Serotype 1,” Archives of Virology, Vol. 144, No. 8, 1999, pp. 1611-1618. doi:10.1007/s007050050614

[19]   J. Smyth and M. McNulty, “Adenoviridae,” In: M. Pattison, P. McMullin, J. Bradbury and D. Alexander, Eds., Poultry Diseases, Elsevier, New York, 2008, pp. 367-381. doi:10.1016/B978-0-7020-2862-5.50036-2

[20]   P. Ketzer, S. F. Haas, S. Engelhardt, J. S. Hartig and D. M. Nettelbeck, “Synthetic Riboswitches for External Regulation of Genes Transferred by Replication-Deficient and Oncolytic Adenoviruses,” Nucleic Acids Research, Vol. 40, No. 21, 2012, p. e167. doi:10.1093/nar/gks734

[21]   B. Klonjkowski, D. Klein, S. Galea, F. Gavard, M. Monteil, L. Duarte, A. Fournier, S. Sayon, K. Gorrna, R. Ertl, N. Cordonnier, P. Sonigo, M. Eloit and J. Richardson, “Gag-Specific Immune Enhancement of Lentiviral Infection after Vaccination with an Adenoviral Vector in an Animal Model of AIDS,” Vaccine, Vol. 27, No. 6, 2009, pp. 928-939. doi:10.1016/j.vaccine.2008.11.086

[22]   H. Murakami, R. Q. Miao, L. Chao and J. Chao, “Adenovirus-Mediated Kallikrein Gene Transfer Inhibits Neointima Formation via Increased Production of Nitric Oxide in Rat Artery,” Immunopharmacology, Vol. 44, No. 1-2, 1999, pp. 137-143. doi:10.1016/S0162-3109(99)00120-4

[23]   O. S. Ramos, A. G. Pose, S. Gomez-Puerta, J. N. Gomez, A. V. Redondo, J. C. A. Benites, L. S. Amaran, N. C. Parra and J. R. T.Alonso, “Avian CD154 Enhances Humoral and Cellular Immune Responses Induced by an Adenovirus Vector-Based Vaccine in Chickens,” Comparative Immunology, Microbiology and Infectious Diseases, Vol. 34, No. 3, 2011, pp. 259-265. doi:10.1016/j.cimid.2010.12.001

[24]   B. Trapnell and M. Gorziglia, “Gene Therapy Using Adenoviral Vectors,” Current Opinion in Biotechnology, Vol. 5, No. 6, 1994, pp. 617-625. doi:10.1016/0958-1669(94)90084-1

[25]   J. L. Imler, “Adenovirus Vectors as Recombinant Viral Vaccines,” Vaccine, Vol. 13, No. 13, 1995, pp. 1143-1151. doi:10.1016/0264-410X(95)00032-V

[26]   W. Russell, “Update on Adenovirus and Its Vectors,” Journal of General Virology, Vol. 81, No. 11, 2000, pp. 2573-2604.

[27]   R. R. Bradley, D. M. Lynch, M. J. Iampietro, E. N. Borducchi and D. H. Barouch, “Adenovirus Serotype 5 Neutralizing Antibodies Target Both Hexon and Fiber Following Vaccination and Natural Infection,” Journal of Virology, Vol. 86, No. 1, 2012, pp. 625-629. doi:10.1128/JVI.06254-11

[28]   M. K. Knowles, D. Roberts, S. Craig, M. Sheen, S. A. Nadin-Davis and A. I. Wandeler, “In Vitro and In Vivo Genetic Stability Studies of a Human Adenovirus Type 5 Recombinant Rabies Glycoprotein Vaccine (ONRAB),” Vaccine, Vol. 27, No. 20, 2009, pp. 2662-2668. doi:10.1016/j.vaccine.2009.02.074

[29]   M. Suleman, S. Galea, F. Gavard, N. Merillon, B. Klonjkowski, E. Tartour and J. Richardson, “Antigen Encoded by Vaccine Vectors Derived from Human Adenovirus Serotype 5 Is Preferentially Presented to CD8+ T Lymphocytes by the CD8+ Dendritic Cell Subset,” Vaccine, Vol. 29, No. 35, 2011, pp. 5892-5903. doi:10.1016/j.vaccine.2011.06.071

[30]   J. Esparza, “The Global HIV Vaccine Enterprise,” International Microbiology, Vol. 8, No. 2, 2005, pp. 93-101.

[31]   A. Lieber, C. Y. He, I. IKirillova and M. A. Kay, “Recombinant Adenoviruses with Large Deletions Generated by Cre-Mediated Excision Exhibit Different Biological Properties Compared with First-Generation Vectors in Vitro and in Vivo,” Journal of Virology, Vol. 70, No. 12, 1996, pp. 8944-8960.

[32]   J. Schaack, “Adenovirus Vectors Deleted for Genes Essential for Viral DNA Replication,” Frontiers in Bioscience, Vol. 10, 2005, pp. 1146-1155. doi:10.2741/1607

[33]   W. Oualikene, P. Gonin and M. Eloit, “Short and Long Term Dissemination of Deletion Mutants of Adenovirus in Permissive (Cotton Rat) and Non-Permissive (Mouse) Species,” Journal of General Virology, Vol. 75, No. 10, 1994, pp. 2765-2768. doi:10.1099/0022-1317-75-10-2765

[34]   L. Peiperl, C. Morgan, Z. Moodie, H. Li, N. Russell, B. S. Graham, G. D. Tomaras, S. C. De Rosa, M. J. McElrath and NIAID Vaccines Trials Network, “Safety and Immunogenicity of a Replication-Defective Adenovirus Type 5 HIV Vaccine in Ad5-Seronegative Persons: A Randomized Clinical Trial (HVTN 054),” PLoS ONE, Vol. 5, No. 10, 2010, p. e13579. doi:10.1371/journal.pone.0013579

[35]   L. Wu, W. Kong and G. Nabel, “Enhanced Breadth of CD4 T-Cell Immunity by DNA Prime and Adenovirus Boost Immunization to Human Immunodeficiency Virus Env and Gag Immunogens,” Journal Virology, Vol. 79, No. 13, 2005, pp. 8024-8031. doi:10.1128/JVI.79.13.8024-8031.2005

[36]   T. Vanniasinkam and H. C. J. Ertl, “Adenoviral Gene Delivery for HIV-1 Vaccination,” Current Gene Therapy, Vol. 5, No. 2, 2005, pp. 203-212. doi:10.2174/1566523053544236

[37]   T. Kojaoghlanian, P. Flomenberg and M. S. Horwitz, “The Impact of Adenovirus Infection on the Immunocompromised Host,” Review of Medical Virology, Vol. 13, No. 3, 2003, pp. 155-171. doi:10.1002/rmv.386

[38]   Y. Zhu, P. Rota, L. Wyatt, A. Tamin, S. Rozenblatt, N. Lerche, B. Moss, W. Bellini and M. McChesney, “Evaluation of Recombinant Vaccinia Virus: Measles Vaccines in Infant Rhesus Macaques with Preexisting Measles Antibody,” Virology, Vol. 276, No. 1, 2000, pp. 202-213. doi:10.1006/viro.2000.0564

[39]   T. Vanniasinkam, S. T. Reddy and H. C. Ertl, “DNA Immunization Using a Non-Viral Promoter,” Virology, Vol. 344, No. 2, 2006, pp. 412-420. doi:10.1016/j.virol.2005.08.040

[40]   H. P. Zhao, J. F. Sun, N. Li, Y. Sun, Y. Wang and H. J. Qiu, “Prime-Boost Immunization Using Alphavirus Replicon and Adenovirus Vectored Vaccines Induces Enhanced Immune Responses against Classical Swine Fever Virus in Mice,” Veterinary Immunology Immunopathology, Vol. 131, No. 3-4, 2009, pp. 158-166. doi:10.1016/j.vetimm.2009.04.003

[41]   P. Holst, C. Ørskov, A. R. Thomsen and J. P. Christensen, “Quality of the Transgene-Specific CD8+ T Cell Response Induced by Adenoviral Vector Immunization Is Critically Influenced by Virus Dose and Route of Vaccination,” Journal of Immunology, Vol. 184, No. 8, 2010, pp. 4431-4439. doi:10.4049/jimmunol.0900537

[42]   A. Patel, Y. Zhang, M. Croyle, K. Tran, M. Gray, J. Strong, H. Feldmann, J. M. Wilson and G. P. Kobinger, “Mucosal Delivery of Adenovirus-Based Vaccine Protects against Ebola Virus Infection in Mice,” Journal of Infectious Diseases, Vol. 196, Suppl. 2, 2007, pp. 413-420. doi:10.1086/520603

[43]   T. J. Bull, S. C. Gilbert, S. Sridhar, R. Linedale, N. Dierkes, K. Sidi-Boumedine and J. Hermon-Taylor, “A Novel Multi-Antigen Virally Vectored Vaccine against Mycobacterium avium subspecies paratuberculosis,” PLoS ONE, Vol. 2, No. 11, 2007, p. e1229. doi:10.1371/journal.pone.0001229

[44]   R. P. Sekaly, “The Failed HIV Merck Vaccine Study: A Step Back or a Launching Point for Future Vaccine Development,” Journal of Experimental Medicine, Vol. 205, No. 1, 2008, pp. 7-12. doi:10.1084/jem.20072681

[45]   K. McCoy, N. Tatsis, B. Korioth-Schmitz, M. O. Lasaro, S. E. Hensley, S. Lin, Y. Li, W. Giles-Davis, A. Cun, D. Zhou, Z. Xiang, N. L. Letvin and H. C. J. Ertl, “Effect of Preexisting Immunity to Adenovirus Human Serotype 5 Antigens on the Immune Responses of Nonhuman Primates to Vaccine Regimens Based on Humanor Chimpanzee-Derived Adenovirus Vectors,” Journal of Virology, Vol. 81, No. 12, 2007, pp. 6594-6604. doi:10.1128/JVI.02497-06

[46]   A. Pandey, N. Singh, S. V. Vemula, L. Couetil, J. M. Katz, R. Donis, S. Sambhara and S. K. Mittal, “Impact of Preexisting Adenovirus Vector Immunity on Immunogenicity and Protection Conferred with an Adenovirus-Based H5N1 Influenza Vaccine,” PLoS ONE, Vol. 7, No. 3, 2012, p. e33428. doi:10.1371/journal.pone.0033428

[47]   J. S. Richardson, M. C. Abou, K. N. Tran, A. Kumar, B. M. Sahai and G. P. Kobinger, “Impact of Systemic or Mucosal Immunity to Adenovirus on Ad-Based Ebola Virus Vaccine Efficacy in Guinea Pigs,” Journal of Infectious Diseases, Vol. 204, Suppl. 3, 2011, pp. S1032-S1042. doi:10.1093/infdis/jir332

[48]   J. F. Engelhardt, L. Litzky and J. M. Wilson, “Prolonged Transgene Expression in Cotton Rat Lung with Recombinant Adenoviruses Defective in E2a,” Human Gene Therapy, Vol. 5, No. 10, 1994, pp. 1217-1229. doi:10.1089/hum.1994.5.10-1217

[49]   A. E. Morelli, 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, “Recombinant Adenovirus Induces Maturation of Dendritic Cells via an NF-Kappab-Dependent Pathway,” Journal of Virology, Vol. 74, No. 20, 2000, pp. 9617-9628.

[50]   L. Trotman, N. Mosberger, M. Fornerod, R. Stidwill and U. Greber, “Import of Adenovirus DNA Involves the Nuclear Pore Complex Receptor CAN/Nup214 and Histone H1,” Nature Cell Biology, Vol. 3, No. 12 2001, pp. 1092-1100. doi:10.1038/ncb1201-1092

[51]   S. Uematsu and S. Akira, “Toll-Like Receptors and Type I Interferons,” Journal of Biological Chemistry, Vol. 282, No. 21, 2007, pp. 15319-15323. doi:10.1074/jbc.R700009200

[52]   P. Verdino, D. A. Witherden, W. L. Havran and I. A. Wilson, “The Molecular Interaction of CAR and JAML Recruits the Central Cell Signal Transducer PI3K,” Science, Vol. 329, No. 5996, 2010, pp. 1210-1214. doi:10.1126/science.1187996

[53]   N. Bessis, F. GarciaCozar, M. C. Boissier, “Immune Responses to Gene Therapy Vectors: Influence on Vector Function and Effector Mechanisms,” Gene Therapy, Vol. 11, Suppl. 1, 2004, pp. S10-S17. doi:10.1038/

[54]   S. Worgall, G. Wolff, E. Falck-Pedersen and R. Crystal, “Innate Immune Mechanisms Dominate Elimination of Adenoviral Vectors Following in Vivo Administration,” Human Gene Therapy, Vol. 8, No. 1, 1997, pp. 37-44. doi:10.1089/hum.1997.8.1-37

[55]   J. M. Hammond, E. S. Jansen, C. J. Morrissy, W. V. Goff, G. C. Meehan, M. M. Williamson, C. Lenghaus, K. W. Sproat, M. E. Andrew, B. E. H. Coupar and M. A. Johnson, “A Prime-Boost Vaccination Strategy Using Naked DNA Followed by Recombinant Porcine Adenovirus Protects Pigs from Classical Swine Fever,” Veterinary Mi-crobiology, Vol. 80, No. 2, 2001, pp. 101-119. doi:10.1016/S0378-1135(00)00388-6

[56]   S. J. Kim, H. K. Kim, Y. W. Han, A. G. Aleyas, J. A. George, H. A. Yoon, D. J. Yoo, K. Kim and S. K. Eo, “Multiple Alternating Immunizations with DNA Vaccine and Replication Incompetent Adenovirus Expressing gB of Pseudorabies Virus Protect Animals against Lethal Virus Challenge,” Journal of Microbiology and Biotechnology, Vol. 18, No. 7, 2008, pp. 1326-1334.

[57]   S. Gogev, K. de Fays, M. F. Versali, S. Gautier and E. Thiry, “Glycol Chitosan Improves the Efficacy of Intranasally Administrated Replication Defective Human Adenovirus Type 5 Expressing Glycoprotein D of Bovine Herpesvirus,” Vaccine, Vol. 22, No. 15-16, 2004, pp. 1946-1953. doi:10.1016/j.vaccine.2003.11.011

[58]   S. D. Perkins, A. J. Williams, L. M. O’Brien, T. R. Laws and R. J. Phillpotts, “CpG Used as an Adjuvant for an Adenovirus-Based Venezuelan Equine Encephalitis Virus Vaccine Increases the Immune Response to the Vector, but not to the Transgene Product,” Viral Immunology, Vol. 21, No. 4, 2008, pp. 451-457. doi:10.1089/vim.2008.0052

[59]   L. Bracci, I. Canini, M. Venditti, M. Spada, S. Puzelli, I. Donatelli, F. Belardelli and E. Proietti, “Type I IFN as a Vaccine Adjuvant for Both Systemic and Mucosal Vaccination against Influenza Virus,” Vaccine, Vol. 24, Suppl. 2, 2006, pp. 56-57. doi:10.1016/j.vaccine.2005.01.121

[60]   H. M. Vordermeier, M. A. Chambers, B. M. Buddle, J. M. Pollock and R. G. Hewinson, “Progress in the Development of Vaccines and Diagnostic Reagents to Control Tuberculosis in Cattle,” The Veterinary Journal, Vol. 171, No. 2, 2006, pp. 229-244.

[61]   H. M. Vordermeier, B. Villarreal-Ramos, P. J. Cockle, M. McAulay, S. G. Rhodes, T. Thacker, S. C. Gilbert, H. McShane, A. V. Hill, Z. Xing and R. G. Hewinson, “Viral Booster Vaccines Improve Mycobacterium Bovis BCG-Induced Protection against Bovine Tuberculosis,” Infection and Immunity, Vol. 77, No. 8, 2009, pp. 3364-3373.

[62]   Z. Xing, C. T. McFarland, J. M. Sallenave, A. Izzo, J. Wang and D. N. McMurray, “Intranasal Mucosal Boosting with an Adenovirus-Vectored Vaccine Markedly Enhances the Protection of BCG-Primed Guinea Pigs against Pulmonary Tuberculosis,” PLoS ONE, Vol. 4, No. 6, 2009, p. e5856. doi:10.1371/journal.pone.0005856

[63]   Y. Sun, N. Li, H. Y. Li, M. Li and H. J. Qiu, “Enhanced Immunity against Classical Swine Fever in Pigs Induced by Prime-Boost Immunization Using an Alphavirus Replicon-Vectored DNA Vaccine and a Recombinant Adenovirus,” Veterinary Immunology and Immunopathology, Vol. 137, No. 1-2, 2010, pp. 20-27. doi:10.1016/j.vetimm.2010.04.005

[64]   J. Schneider, S. C. Gilbert, C. M. Hannan, P. Dégano, E. Prieur, E. G. Sheu, M. Plebanski and A. V. Hill, “Induction of CD8+ T Cells Using Heterologous Prime-Boost Immunisation Strategies,” Immunological Reviews, Vol. 170, No. 1, 1999, pp. 29-38. doi:10.1111/j.1600-065X.1999.tb01326.x

[65]   A. de Mare, A. J. Lambeck, J. Regts, G. M.van Dam, H. W. Nijman, H. Snippe, J. Wilschut and T. Daemen, “Viral Vector-Based Prime-Boost Immunization Regimens: A Possible Involvement of T-Cell Competition,” Gene Therapy, Vol. 15, No. 6, 2008, pp. 393-403. doi:10.1038/

[66]   B. Asefa, N. Korokhov and F. Lemiale, “Heterologous HIV-Based Lentiviral/Adenoviral Vectors Immunizations Result in Enhanced HIV-Specific Immunity,” Vaccine, Vol. 28, No. 20, 2010, pp. 3617-3624. doi:10.1016/j.vaccine.2009.12.047

[67]   E. K. Roediger, K. Kugathasan, X. Zhang, B. D. Lichty and Z. Xing, “Heterologous Boosting of Recombinant Adenoviral Prime Immunization with a Novel Vesicular Stomatitis Virus-Vectored Tuberculosis Vaccine,” Molecular Therapy, Vol. 16, No. 6, 2008, pp. 1161-1169. doi:10.1038/mt.2008.59

[68]   F. H. J. Top, B. A. Dudding, P. K. Russel and E. L. Buescher, “Control of Respiratory Disease in Recruits with Types 4 and 7 Adenovirus Vaccines,” American Journal of Epidemiology, Vol. 94, No. 2, 1971, pp. 142-146.

[69]   B. Zeshan, L. Zhang, J. Bai, X. Wang, J. Xu and P. Jiang, “Immunogenicity and Protective Efficacy of a Replication-Defective Infectious Bronchitis Virus Vaccine Using an Adenovirus Vector and Administered in ovo,” Journal of Virology Methods, Vol. 166, No. 1-2, 2010, pp. 54-59. doi:10.1016/j.jviromet.2010.02.019

[70]   B. Barefoot, N. J. Thornburg, D. H. Barouch, J. S. Yu, C. Sample, R. E. Johnston, H. X. Liao, T. B. Kepler, B. F. Haynes and E. Ramsburg, “Comparison of Multiple Vaccine Vectors in a Single Heterologous Prime-Boost Trial,” Vaccine, Vol. 26, No. 48, 2008, pp. 6108-6118. doi:10.1016/j.vaccine.2008.09.007

[71]   R. C. Carlisle, S. S. Briggs, A. B. Hale, N. K. Green, K. D. Fisher, T. Etrych, K. Ulbrich, V. Mautner and L. W. Seymour, “Use of Synthetic Vectors for Neutralizing Antibody Resistant Delivery of Replicating Adenovirus DNA,” Gene Therapy, Vol. 13, No. 22, 2006, pp. 1579-1586. doi:10.1038/

[72]   J. Millar, D. Dissanayake, T. C. Yang, N. Grinshtein, C. Evelegh, Y. Wan and J. Bramson, “The Magnitude of the CD8+ T Cell Response Produced by Recombinant Virus Vectors Is a Function of Both the Antigen and the Vector,” Cellular Immunology, Vol. 250, No. 1-2, 2007, pp. 55-67. doi:10.1016/j.cellimm.2008.01.005

[73]   L. Fischer, J. P. Tronel, C. Pardo-David, P. Tanner, G. Colombet, J. Minke and J. C. Audonnet, “Vaccination of Puppies Born to Immune Dams with a Canine Adenovirus-Based Vaccine Protects against a Canine Distemper Virus Challenge,” Vaccine, Vol. 20, No. 29-30, 2002, pp. 3485-3497. doi:10.1016/S0264-410X(02)00344-4

[74]   Z. Q. Xiang, G. P. Gao, A. Reyes-Sandoval, Y. Li, J. M. Wilson and H. C. Ertl, “Oral Vaccination of Mice with Adenoviral Vectors Is not Impaired by Preexisting Immunity to the Vaccine Carrier,” Journal of Virology, Vol. 77, No. 20, 2003, pp. 10780-10789. doi:10.1128/JVI.77.20.10780-10789.2003

[75]   R. D. Wesley and K. M. Lager, “Overcoming Maternal Antibody Interference by Vaccination with Human Adenovirus 5 Recombinant Viruses Expressing the Hemagglutinin and the Nucleoprotein of Swine Influenza Virus,” Veterinary Microbiology, Vol. 118, No. 1-2, 2006, pp. 67-75. doi:10.1016/j.vetmic.2006.07.014

[76]   W. Chen, M. Liu, Y. Jiao, W. Yan, X. Wei, J. Chen, L. Fei, Y. Liu, X. Zuo, F. Yang, Y. Lu and Z. Zheng, “Adenovirus-Mediated RNA Interference against Foot-and-Mouth Disease Virus Infection Both in Vitro and in Vivo,” Journal of Virology, Vol. 80, No. 7, 2006, pp. 3559-3566. doi:10.1128/JVI.80.7.3559-3566.2006

[77]   Y. Li, K. Reddy, S. M. Reid, W. J. Cox, I. H. Brown, P. Britton, V. Nair and M. Iqbal, “Recombinant Herpesvirus of Turkeys as a Vector-Based Vaccine against Highly Pathogenic H7N1 Avian Influenza and Marek’s Disease,” Vaccine, Vol. 29, No. 46, 2011, pp. 8257-8266. doi:10.1016/j.vaccine.2011.08.115

[78]   R. Hu, S. Zhang, A. R. Fooks, H. Yuan, Y. Liu, H. Li, C. Tu, X. Xia and Y. Xiao, “Prevention of Rabies Virus Infection in Dogs by a Recombinant Canine Adenovirus Type-2 Encoding the Rabies Virus Glycoprotein,” Microbes and Infection, Vol. 8, No. 4, 2006, pp. 1090-1097. doi:10.1016/j.micinf.2005.11.007

[79]   P. Reddy, N. Idamakanti, C. Pyne, A. Zakhartchouk, D. L. Godson, Z. Papp, M. E. Baca-Estrada, L. A. Babiuk, G. K. Mutwiri and S. K. Tikoo, “The Immunogenicity and Efficacy of Replication-Defective and Replication-Competent Bovine Adenovirus-3 Expressing Bovine Herpesvirus-1 Glycoprotein gD in Cattle,” Veterinary Immunology and Immunopathology, Vol. 76, No. 3-4, 2000, pp. 257-268. doi:10.1016/S0165-2427(00)00217-8

[80]   T. Tuboly and E. Nagy, “Construction and Characterization of Recombinant Porcine Adenovirus Serotype 5 Expressing the Transmissible Gastroenteritis Virus Spike Gene,” Journal of General Virology, Vol. 82, No. 1, 2001, pp. 183-190.

[81]   J. S. Rothel, D. B. Boyle, G. W. Both, A. D. Pye, J. G. Waterkeyn, P. R. Wood and M. W. Lightowlers, “Sequential Nucleic Acid and Recombinant Adenovirus Vaccination Induces Host-Protective Immune Responses against Taenia Ovis Infection in Sheep,” Parasite Immunology,Vol. 19, No. 5, 1997, pp. 221-227. doi:10.1046/j.1365-3024.1997.d01-200.x

[82]   A. Francois, C. Chevalier, B. Delmas, N. Eterradossi, D. Toquin, G. Rivallan and P. Langlois, “Avian Adenovirus CELO Recombinants Expressing VP2 of Infectious Bursal Disease Virus Induce Protection against Bursal Disease in Chickens,” Vaccine, Vol. 22, No. 17-18, 2004, pp. 2351-2360. doi:10.1016/j.vaccine.2003.10.039

[83]   J. Domenech, J. Lubroth and K. Sumption, “Immune Protection in Animals: The Examples of Rinderpest and Foot-and-Mouth Disease,” Journal of Comparative Pathology, Vol. 142, Suppl. 1, 2010, pp. S120-S124. doi:10.1016/j.jcpa.2009.11.003

[84]   J. G. Heldens, J. R. Patel, N. Chanter, G. J. Ten Thij, M. Gravendijck, V. E. Schijns, A. Langen and T. P. Schetters, “Veterinary Vaccine Development from an Industrial Perspective,” The Veterinary Journal, Vol. 178, No. 1, 2008, pp. 7-20. doi:10.1016/j.tvjl.2007.11.009

[85]   P. H. Flore, “Commercialization of Veterinary Viral Vaccines,” Animal Health Research Reviews, Vol. 5, No. 2, 2004, pp. 239-242. doi:10.1079/AHR200475

[86]   A. K. Shen, “The U.S. Vaccine and Immunization Enterprise: Working to Sustain and Foster Vaccine Innovation,” Human Vaccines, Vol. 5, No. 10, 2009, pp. 649-653. doi:10.4161/hv.5.10.9215

[87]   D. A. Brake, M. McIlhaney, T. Miller, K. Christianson, A. Keene, G. Lohnas, C. Purcell, J. Neilan, C. Schutta, J. Barrera, T. Burrage, D. E. Brough and B. T. Butman, “Human Adenovirus-Vectored Foot-and-Mouth Disease Vaccines: Establishment of a Vaccine Product Profile Through in Vitro Testing,” Developments in Biologicals (Basel), Vol. 134, 2012, pp. 123-133.

[88]   M. J. Grubman, M. P. Moraes, C. Schutta, J. Barrera, J. Neilan, D. Ettyreddy, B. T. Butman, D. E. Brough and D. A. Brake, “Adenovirus Serotype 5-Vectored Foot-and-Mouth Disease Subunit Vaccines: The First Decade,” Future Virology, Vol. 5, No. 1, 2010, pp. 51-64. doi:10.2217/fvl.09.68

[89]   M. Bublot, N. Pritchard, D. E. Swayne, P. Selleck, K. Karaca, D. L. Suarez, J. C. Audonnet and T. R. Mickle, “Development and Use of Fowlpox Vectored Vaccines for Avian Influenza,” Annals of the New York Academy of Sciences, Vol. 1081, No. 1, 2006, pp. 193-201. doi:10.1196/annals.1373.023

[90]   J. Coon, M. Johnston, J. Minke, R. Pruett, S. Thompson and D. Carithers, “Analysis of Recombinant Canarypox Vectored West Nile Virus Vaccine Stability Post-Reconstitution,” International Journal of Applied Research in Veterinary Medicine, Vol. 4, No. 2, 2006, pp. 115-120.

[91]   H. Poulet, S. Brunet, C. Boularand, A. L. Guiot, V. Leroy, J. Tartaglia, J. Minke, J. C. Audonnet and P. Desmettre, “Efficacy of a Canarypox Virus-Vectored Vaccine Against Feline Leukaemia,” Veterinary Record, Vol. 153, No. 5, 2003, pp. 141-145. doi:10.1136/vr.153.5.141

[92]   United States Department of Agriculture, “Veterinary Biological Products-Licensees and Permittees,” 2011.

[93]   J. Esparza, “Progress in the Development of an Adenovirus 26 Vector Platform for HIV Vaccines,” Expert Reviews in Vaccines, Vol. 12, No. 5, 2013, pp. 477-480. doi:10.1586/erv.13.26

[94]   Z. C. Hartman, D. M. Appledorn and A. Amalfitano, “Adenovirus Vector Induced Innate Immune Responses: Impact upon Efficacy and Toxicity in Gene Therapy and Vaccine applications,” Virus Research, Vol. 132, No. 1-2, 2008, pp. 1-14. doi:10.1016/j.virusres.2007.10.005

[95]   L. S. Wyatt, P. L. Earl, W. Xiao, J. L. Americo, C. A. Cotter, J. Vogt and B. Moss, “Elucidating and Minimizing the Loss by Recombinant Vaccinia Virus of Human Immuno-deficiency Virus Gene Expression Resulting from Spontaneous Mutations and Positive Selection,” Journal of Virology, Vol. 83, No. 14, 2009, pp. 7176-7184.