Vaccines within vaccines: The use of adenovirus types 4 and 7 as influenza vaccine vectors

Human Vaccines and Immunotherapeutics

Volumn 10, Issue 3, 2014, Pages 544-556

  Weaver, EricA ^a  

^a MAYO CLINIC   (United States)

Author keywords

Adenovirus; Adenovirus type 4; Adenovirus type 7; Centralized gene; Hemagglutinin; Influenza; Vaccine; Viral vector

Indexed keywords

ADENOVIRUS VECTOR; INFLUENZA VACCINE; MEMBRANE COFACTOR PROTEIN; VIRUS HEMAGGLUTININ; ADENOVIRUS VACCINE; DRUG CARRIER; INFLUENZA VIRUS HEMAGGLUTININ; RECOMBINANT VACCINE;

ADENOVIRUS; ADENOVIRUS 4; ADENOVIRUS 7; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG EFFICACY; FEMALE; FUSION GENE; GFPLUC GENE; H1 GENE; IN VIVO STUDY; INFECTION PREVENTION; INFLUENZA A (H1N1); MOLECULAR CLONING; MOUSE; NONHUMAN; VIRAL GENE DELIVERY SYSTEM; VIRUS GENE; VIRUS IMMUNITY; ANIMAL; BAGG ALBINO MOUSE; DISEASE MODEL; GENE VECTOR; GENETICS; IMMUNOLOGY; ORTHOMYXOVIRIDAE INFECTIONS; SURVIVAL ANALYSIS; TRANSGENIC MOUSE;

ADENOVIRUS VACCINES; ANIMALS; DISEASE MODELS, ANIMAL; DRUG CARRIERS; FEMALE; GENETIC VECTORS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; INFLUENZA VACCINES; MICE, INBRED BALB C; MICE, TRANSGENIC; ORTHOMYXOVIRIDAE INFECTIONS; SURVIVAL ANALYSIS; VACCINES, SYNTHETIC;

EID: 84898471075     PISSN: 21645515     EISSN: 2164554X     Source Type: Journal    
DOI: 10.4161/hv.27238     Document Type: Article

References (45)

1. Dudding BA, Top FH Jr., Winter PE, Buescher EL, Lamson TH, Leibovitz A. Acute respiratory disease in military trainees: the adenovirus surveillance program, 1966-1971. Am J Epidemiol 1973; 97:187-98; PMID:4348245
2. Kitchen LW, Vaughn DW. Role of U.S. military research programs in the development of U.S.-licensed vaccines for naturally occurring infectious diseases. Vaccine 2007; 25:7017-30; PMID:17728025; http://dx.doi.org/10.1016/j. vaccine.2007.07.030
3. Gaydos CA, Gaydos JC. Adenovirus vaccines in the U.S. military. Mil Med 1995; 160:300-4; PMID:7659229
4. Buescher EL. Respiratory disease and the adenoviruses. Med Clin North Am 1967; 51:769-79; PMID:4290351
5. Hyer RN, Howell MR, Ryan MAK, Gaydos JC. Cost-effectiveness analysis of reacquiring and using adenovirus types 4 and 7 vaccines in naval recruits. Am J Trop Med Hyg 2000; 62:613-8; PMID:11289673
6. Gurwith M, Lock M, Taylor EM, Ishioka G, Alexander J, Mayall T, Ervin JE, Greenberg RN, Strout C, Treanor JJ, et al. Safety and immunogenicity of an oral, replicating adenovirus serotype 4 vector vaccine for H5N1 influenza: a randomised, double-blind, placebo-controlled, phase 1 study. Lancet Infect Dis 2013; 13:238-50; PMID:23369412; http://dx.doi.org/10.1016/S1473-3099(12)70345-6
7. Hoke CH Jr., Snyder CE Jr. History of the restoration of adenovirus type 4 and type 7 vaccine, live oral (Adenovirus Vaccine) in the context of the Department of Defense acquisition system. Vaccine 2013; 31:1623-32; PMID:23291475; http://dx.doi.org/10.1016/j.vaccine.2012.12.029
8. Santra S, Sun Y, Korioth-Schmitz B, Fitzgerald J, Charbonneau C, Santos G, Seaman MS, Ratcliffe SJ, Montefiori DC, Nabel GJ, et al. Heterologous prime/boost immunizations of rhesus monkeys using chimpanzee adenovirus vectors. Vaccine 2009; 27:5837-45; PMID:19660588; http://dx.doi.org/10.1016/j.vaccine. 2009.07.050
9. Weaver EA, Nehete PN, Nehete BP, Buchl SJ, Palmer D, Montefiori DC, Ng P, Sastry KJ, Barry MA. Protection against Mucosal SHIV Challenge by Peptide and Helper-Dependent Adenovirus Vaccines. Viruses 2009; 1:920-38; PMID:20107521; http://dx.doi.org/10.3390/v1030920
10. Weaver EA, Nehete PN, Buchl SS, Senac JS, Palmer D, Ng P, Sastry KJ, Barry MA. Comparison of replication-competent, first generation, and helper-dependent adenoviral vaccines. PLoS One 2009; 4:e5059; PMID:19333387; http://dx.doi.org/10.1371/journal.pone.0005059
11. Weaver EA, Rubrum AM, Webby RJ, Barry MA. Protection against divergent influenza H1N1 virus by a centralized influenza hemagglutinin. PLoS One 2011; 6:e18314; PMID:21464940; http://dx.doi.org/10.1371/journal.pone.0018314
12. Lemckert AA, Sumida SM, Holterman L, Vogels R, Truitt DM, Lynch DM, Nanda A, Ewald BA, Gorgone DA, Lifton MA, et al. 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 2005; 79:9694-701; PMID:16014931; http://dx.doi.org/10.1128/JVI.79.15.9694-9701.2005
13. Tan WG, Jin HT, West EE, Penaloza-MacMaster P, Wieland A, Zilliox MJ, McElrath MJ, Barouch DH, Ahmed R. Comparative analysis of simian immunodeficiency virus gag-specific effector and memory CD8+ T cells induced by different adenovirus vectors. J Virol 2013; 87:1359-72; PMID:23175355; http://dx.doi.org/10.1128/JVI.02055-12
14. Abbink P, Lemckert AA, Ewald BA, Lynch DM, Denholtz M, Smits S, Holterman L, Damen I, Vogels R, Thorner AR, et al. Comparative seroprevalence and immunogenicity of six rare serotype recombinant adenovirus vaccine vectors from subgroups B and D. J Virol 2007; 81:4654-63; PMID:17329340; http://dx.doi.org/ 10.1128/JVI.02696-06
15. Barouch DH, Kik SV, Weverling GJ, Dilan R, King SL, Maxfield LF, Clark S, Ng'ang'a D, Brandariz KL, Abbink P, et al. International seroepidemiology of adenovirus serotypes 5, 26, 35, and 48 in pediatric and adult populations. Vaccine 2011; 29:5203-9; PMID:21619905; http://dx.doi.org/10.1016/j.vaccine. 2011.05.025
16. Mast TC, Kierstead L, Gupta SB, Nikas AA, Kallas EG, Novitsky V, Mbewe B, Pitisuttithum P, Schechter M, Vardas E, et al. 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; 28:950-7; PMID:19925902; http://dx.doi.org/10.1016/j.vaccine.2009.10.145
17. Ludwig SL, Brundage JF, Kelley PW, Nang R, Towle C, Schnurr DP, Crawford-Miksza L, Gaydos JC. Prevalence of antibodies to adenovirus serotypes 4 and 7 among unimmunized US Army trainees: results of a retrospective nationwide seroprevalence survey. J Infect Dis 1998; 178:1776-8; PMID:9815232; http://dx.doi.org/10.1086/314498
18. Chengalvala M, Lubeck MD, Davis AR, Mizutani S, Molnar-Kimber K, Morin J, Hung PP. Evaluation of adenovirus type 4 and type 7 recombinant hepatitis B vaccines in dogs. Vaccine 1991; 9:485-90; PMID:1832806; http://dx.doi.org/10. 1016/0264-410X(91)90033-3
19. Lubeck MD, Davis AR, Chengalvala M, Natuk RJ, Morin JE, Molnar-Kimber K, Mason BB, Bhat BM, Mizutani S, Hung PP, et al. Immunogenicity and efficacy testing in chimpanzees of an oral hepatitis B vaccine based on live recombinant adenovirus. Proc Natl Acad Sci U S A 1989; 86:6763-7; PMID:2570422; http://dx.doi.org/10.1073/pnas.86.17.6763
20. Natuk RJ, Lubeck MD, Chanda PK, Chengalvala M, Wade MS, Murthy SC, Wilhelm J, Vernon SK, Dheer SK, Mizutani S, et al. Immunogenicity of recombinant human adenovirus-human immunodeficiency virus vaccines in chimpanzees. AIDS Res Hum Retroviruses 1993; 9:395-404; PMID:8318268; http://dx.doi.org/10.1089/aid. 1993.9.395
21. Alexander J, Ward S, Mendy J, Manayani DJ, Farness P, Avanzini JB, Guenther B, Garduno F, Jow L, Snarsky V, et al. Pre-clinical evaluation of a replication-competent recombinant adenovirus serotype 4 vaccine expressing influenza H5 hemagglutinin. PLoS One 2012; 7:e31177; PMID:22363572; http://dx.doi.org/10.1371/journal.pone.0031177
22. Hsu KH, Lubeck MD, Davis AR, Bhat RA, Selling BH, Bhat BM, Mizutani S, Murphy BR, Collins PL, Chanock RM, et al. Immunogenicity of recombinant adenovirus-respiratory syncytial virus vaccines with adenovirus types 4, 5, and 7 vectors in dogs and a chimpanzee. J Infect Dis 1992; 166:769-75; PMID:1527411; http://dx.doi.org/10.1093/infdis/166.4.769
23. Artenstein AW. Vaccines for military use. Vaccine 2009; 27(Suppl 4):D16-22; PMID:19837279; http://dx.doi.org/10.1016/j.vaccine.2009.07.044
24. Wold WS, Gooding LR. Region E3 of adenovirus: a cassette of genes involved in host immunosurveillance and virus-cell interactions. Virology 1991; 184:1-8; PMID:1831308; http://dx.doi.org/10.1016/0042-6822(91)90815-S
25. Lesokhin AM, Delgado-Lopez F, Horwitz MS. Inhibition of chemokine expression by adenovirus early region three (E3) genes. J Virol 2002; 76:8236-43; PMID:12134029; http://dx.doi.org/10.1128/JVI.76.16.8236-8243.2002
26. Horwitz MS, Efrat S, Christen U, von Herrath MG, Oldstone MB. Adenovirus E3 MHC inhibitory genes but not TNF/Fas apoptotic inhibitory genes expressed in beta cells prevent autoimmune diabetes. Proc Natl Acad Sci U S A 2009; 106:19450-4; PMID:19887639; http://dx.doi.org/10.1073/pnas.0910648106
27. Koehler DR, Martin B, Corey M, Palmer D, Ng P, Tanswell AK, Hu J. Readministration of helper-dependent adenovirus to mouse lung. Gene Ther 2006; 13:773-80; PMID:16437131; http://dx.doi.org/10.1038/sj.gt.3302712
28. Croyle MA, Chirmule N, Zhang Y, Wilson JM. PEGylation of E1-deleted adenovirus vectors allows significant gene expression on readministration to liver. Hum Gene Ther 2002; 13:1887-900; PMID:12396620; http://dx.doi.org/10. 1089/104303402760372972
29. Kuzmin AI, Galenko O, Eisensmith RC. An immunomodulatory procedure that stabilizes transgene expression and permits readministration of E1-deleted adenovirus vectors. Mol Ther 2001; 3:293-301; PMID:11273770; http://dx.doi.org/10.1006/mthe.2000.0258
30. Nagao S, Kuriyama S, Okuda H, Tominaga K, Nakatani T, Tsujinoue H, Yoshiji H, Fukui H. Adenovirus-mediated gene transfer into tumors: evaluation of direct readministration of an adenoviral vector into subcutaneous tumors of immunocompetent mice. Int J Oncol 2001; 18:57-65; PMID:11115539
31. Chirmule N, Raper SE, Burkly L, Thomas D, Tazelaar J, Hughes JV, Wilson JM. Readministration of adenovirus vector in nonhuman primate lungs by blockade of CD40-CD40 ligand interactions. J Virol 2000; 74:3345-52; PMID:10708452; http://dx.doi.org/10.1128/JVI.74.7.3345-3352.2000
32. McClane SJ, Chirmule N, Burke CV, Raper SE. Characterization of the immune response after local delivery of recombinant adenovirus in murine pancreas and successful strategies for readministration. Hum Gene Ther 1997; 8:2207-16; PMID:9449374; http://dx.doi.org/10.1089/hum.1997.8.18-2207
33. Wang H, Li ZY, Liu Y, Persson J, Beyer I, Möller T, Koyuncu D, Drescher MR, Strauss R, Zhang XB, et al. Desmoglein 2 is a receptor for adenovirus serotypes 3, 7, 11 and 14. Nat Med 2011; 17:96-104; PMID:21151137; http://dx.doi.org/10.1038/nm.2270
34. Hartman ZC, Appledorn DM, Serra D, Glass O, Mendelson TB, Clay TM, Amalfitano A. Replication-attenuated Human Adenoviral Type 4 vectors elicit capsid dependent enhanced innate immune responses that are partially dependent upon interactions with the complement system. Virology 2008; 374:453-67; PMID:18280530; http://dx.doi.org/10.1016/j.virol.2008.01.017
35. Oglesby TJ, Allen CJ, Liszewski MK, White DJ, Atkinson JP. Membrane cofactor protein (CD46) protects cells from complement-mediated attack by an intrinsic mechanism. J Exp Med 1992; 175:1547-51; PMID:1588280; http://dx.doi.org/10.1084/jem.175.6.1547
36. Wang H, Beyer I, Persson J, Song H, Li Z, Richter M, Cao H, van Rensburg R, Yao X, Hudkins K, et al. A new human DSG2-transgenic mouse model for studying the tropism and pathology of human adenoviruses. J Virol 2012; 86:6286-302; PMID:22457526; http://dx.doi.org/10.1128/JVI.00205-12
37. Kuschner RA, Russell KL, Abuja M, Bauer KM, Faix DJ, Hait H, Henrick J, Jacobs M, Liss A, Lynch JA, et al.; Adenovirus Vaccine Efficacy Trial Consortium. A phase 3, randomized, double-blind, placebo-controlled study of the safety and efficacy of the live, oral adenovirus type 4 and type 7 vaccine, in U.S. military recruits. Vaccine 2013; 31:2963-71; PMID:23623865; http://dx.doi.org/10.1016/j.vaccine.2013.04.035
38. Nam JH, Na HN, Atkinson RL, Dhurandhar NV. (2013) Genomic stability of adipogenic human adenovirus 36. Int J Obes (Lond).
39. Murray CJ, Rosenfeld LC, Lim SS, Andrews KG, Foreman KJ, Haring D, Fullman N, Naghavi M, Lozano R, Lopez AD. Global malaria mortality between 1980 and 2010: a systematic analysis. Lancet 2012; 379:413-31; PMID:22305225; http://dx.doi.org/10.1016/S0140-6736(12)60034-8
40. Fukuda MM, Klein TA, Kochel T, Quandelacy TM, Smith BL, Villinski J, Bethell D, Tyner S, Se Y, Lon C, et al.; AFHSC-GEIS Malaria and Vector Borne Infections Writing Group. Malaria and other vector-borne infection surveillance in the U.S. Department of Defense Armed Forces Health Surveillance Center-Global Emerging Infections Surveillance program: review of 2009 accomplishments. BMC Public Health 2011; 11(Suppl 2):S9; PMID:21388569; http://dx.doi.org/10.1186/ 1471-2458-11-S2-S9
41. Whitman TJ, Coyne PE, Magill AJ, Blazes DL, Green MD, Milhous WK, Burgess TH, Freilich D, Tasker SA, Azar RG, et al. An outbreak of Plasmodium falciparum malaria in U.S. Marines deployed to Liberia. Am J Trop Med Hyg 2010; 83:258-65; PMID:20682864; http://dx.doi.org/10.4269/ajtmh.2010.09-0774
42. Chuang I, Sedegah M, Cicatelli S, Spring M, Polhemus M, Tamminga C, Patterson N, Guerrero M, Bennett JW, McGrath S, et al. DNA prime/ Adenovirus boost malaria vaccine encoding P. falciparum CSP and AMA1 induces sterile protection associated with cell-mediated immunity. PLoS One 2013; 8:e55571; PMID:23457473; http://dx.doi.org/10.1371/journal.pone.0055571
43. Vogels R, Zuijdgeest D, van Rijnsoever R, Hartkoorn E, Damen I, de Béthune MP, Kostense S, Penders G, Helmus N, Koudstaal W, et al. 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; 77:8263-71; PMID:12857895; http://dx.doi.org/10.1128/ JVI.77.15.8263-8271.2003
44. Berge TO, England B, Mauris C, Shuey HE, Lennette EH. Etiology of acute respiratory disease among service personnel at Fort Ord, California. Am J Hyg 1955; 62:283-94; PMID:13268418
45. Sprangers MC, Lakhai W, Koudstaal W, Verhoeven M, Koel BF, Vogels R, Goudsmit J, Havenga MJ, Kostense S. Quantifying adenovirus-neutralizing antibodies by luciferase transgene detection: addressing preexisting immunity to vaccine and gene therapy vectors. J Clin Microbiol 2003; 41:5046-52; PMID:14605137; http://dx.doi.org/10.1128/JCM.41.11.5046-5052.2003