Beyond oncolytics: E1B55K-deleted adenovirus as a vaccine delivery vector

PLoS ONE

Volumn 11, Issue 7, 2016, Pages

  Thomas, Michael A ^a,b   Nyanhete, Tinashe ^a,c   Tuero, Iskra ^a   Venzon, David ^a   Robert Guroff, Marjorie ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b HOWARD UNIVERSITY   (United States)

^c DUKE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 13; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR; INTERLEUKIN 4; INTERLEUKIN 6; INTERLEUKIN 7; INTERLEUKIN 8; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; ONCOLYTIC ADENOVIRUS; RANTES; TUMOR NECROSIS FACTOR ALPHA; DNA VACCINE; E1B55K PROTEIN, ADENOVIRUS; LONTUCIREV; ONCOLYTIC VIRUS; VIRAL PROTEIN; VIRUS VACCINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY TITER; ANTIGEN BINDING; ARTICLE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; E1B55K GENE; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE DELETION; HUMAN; HUMAN CELL; HUMORAL IMMUNITY; IMMUNOGENICITY; INNATE IMMUNITY; MOUSE; NONHUMAN; ONCOGENE; ONCOLYTIC VIROTHERAPY; PROGENY; PROTEIN DOMAIN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; VIRION; A-549 CELL LINE; ADENOVIRIDAE; ANIMAL; BAGG ALBINO MOUSE; CELL LINE; CHLOROCEBUS AETHIOPS; GENETICS; HEK293 CELL LINE; HELA CELL LINE; HUMAN ADENOVIRUS C; METABOLISM; SUPPLY AND DISTRIBUTION; T LYMPHOCYTE; WESTERN BLOTTING;

A549 CELLS; ADENOVIRIDAE; ADENOVIRUSES, HUMAN; ANIMALS; BLOTTING, WESTERN; CELL LINE; CERCOPITHECUS AETHIOPS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; HEK293 CELLS; HELA CELLS; HUMANS; MICE; MICE, INBRED BALB C; ONCOLYTIC VIRUSES; T-LYMPHOCYTES; VACCINES, DNA; VIRAL PROTEINS; VIRAL VACCINES;

EID: 84979210048     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0158505     Document Type: Article

References (29)

1. Patterson LJ, Robert-Guroff M. Replicating adenovirus vector prime/protein boost strategies for HIV vaccine development. Expert Opin Biol Ther. 2008; 8(9):1347-63. doi: 10.1517/14712598.8.9.1347 PMID: 18694354; PubMed Central PMCID: PMC2538611.
2. Lubeck MD, Natuk R, Myagkikh M, Kalyan N, Aldrich K, Sinangil F, et al. Long-term protection of chimpanzees against high-dose HIV-1 challenge induced by immunization. Nat Med. 1997; 3(6):651-8. PMID: 9176492.
3. Robert-Guroff M, Kaur H, Patterson LJ, Leno M, Conley AJ, McKenna PM, et al. Vaccine protection against a heterologous, non-syncytium-inducing, primary human immunodeficiency virus. J Virol. 1998; 72(12):10275-80. PMID: 9811775; PubMed Central PMCID: PMC110613.
4. Patterson LJ, Malkevitch N, Venzon D, Pinczewski J, Gomez-Roman VR, Wang L, et al. Protection against mucosal simian immunodeficiency virus SIV(mac251) challenge by using replicating adenovirus-SIV multigene vaccine priming and subunit boosting. J Virol. 2004; 78(5):2212-21. PMID: 14963117; PubMed Central PMCID: PMC369221.
5. Malkevitch NV, Patterson LJ, Aldrich MK, Wu Y, Venzon D, Florese RH, et al. Durable protection of rhesus macaques immunized with a replicating adenovirus-SIV multigene prime/protein boost vaccine regimen against a second SIVmac251 rectal challenge: role of SIV-specific CD8+ T cell responses. Virology. 2006; 353(1):83-98. doi: 10.1016/j.virol.2006.05.012 PMID: 16814356.
6. Demberg T, Florese RH, Heath MJ, Larsen K, Kalisz I, Kalyanaraman VS, et al. A replication-competent adenovirus-human immunodeficiency virus (Ad-HIV) tat and Ad-HIV env priming/Tat and envelope protein boosting regimen elicits enhanced protective efficacy against simian/human immunodeficiency virus SHIV89.6P challenge in rhesus macaques. J Virol. 2007; 81(7):3414-27. doi: 10.1128/JVI.02453-06 PMID: 17229693; PubMed Central PMCID: PMC1866031.
7. Bogers WM, Davis D, Baak I, Kan E, Hofman S, Sun Y, et al. Systemic neutralizing antibodies induced by long interval mucosally primed systemically boosted immunization correlate with protection from mucosal SHIV challenge. Virology. 2008; 382(2):217-25. PMID: 18947849. doi: 10.1016/j.virol.2008.09.016
8. Alexander J, Ward S, Mendy J, Manayani DJ, Farness P, Avanzini JB, et al. Pre-clinical evaluation of a replication-competent recombinant adenovirus serotype 4 vaccine expressing influenza H5 hemagglutinin. PLoS One. 2012; 7(2):e31177. doi: 10.1371/journal.pone.0031177 PMID: 22363572; PubMed Central PMCID: PMC3281928.
9. Gurwith M, Lock M, Taylor EM, Ishioka G, Alexander J, Mayall T, 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. doi: 10.1016/S1473-3099(12)70345-6 PMID: 23369412.
10. Alexander J, Mendy J, Vang L, Avanzini JB, Garduno F, Manayani DJ, et al. Pre-clinical development of a recombinant, replication-competent adenovirus serotype 4 vector vaccine expressing HIV-1 envelope 1086 clade C. PLoS One. 2013; 8(12):e82380. doi: 10.1371/journal.pone.0082380 PMID: 24312658; PubMed Central PMCID: PMC3849430.
11. Garber K. China approves world's first oncolytic virus therapy for cancer treatment. J Natl Cancer Inst. 2006; 98(5):298-300. doi: 10.1093/jnci/djj111 PMID: 16507823.
12. Crompton AM, Kirn DH. From ONYX-015 to armed vaccinia viruses: the education and evolution of oncolytic virus development. Curr Cancer Drug Targets. 2007; 7(2):133-9. PMID: 17346104.
13. Fouts TR, Tuskan R, Godfrey K, Reitz M, Hone D, Lewis GK, et al. Expression and characterization of a single-chain polypeptide analogue of the human immunodeficiency virus type 1 gp120-CD4 receptor complex. J Virol. 2000; 74(24):11427-36. PMID: 11090138.
14. Thomas MA, Song R, Demberg T, Vargas-Inchaustegui DA, Venzon D, Robert-Guroff M. Effects of the deletion of early region 4 (E4) open reading frame 1 (orf1), orf1-2, orf1-3 and orf1-4 on virus-host cell interaction, transgene expression, and immunogenicity of replicating adenovirus HIV vaccine vectors. PLoS One. 2013; 8(10):e76344. doi: 10.1371/journal.pone.0076344 PMID: 24143187; PubMed Central PMCID: PMC3797075.
15. Thomas MA, Tuero I, Demberg T, Vargas-Inchaustegui DA, Musich T, Xiao P, et al. HIV-1 CD4-induced (CD4i) gp120 epitope vaccines promote B and T-cell responses that contribute to reduced viral loads in rhesus macaques. Virology. 2014;471-473:81-92. doi: 10.1016/j.virol.2014.10.001 PMID: 25461534; PubMed Central PMCID: PMC4312258.
16. Miller DL, Rickards B, Mashiba M, Huang W, Flint SJ. The adenoviral E1B 55-kilodalton protein controls expression of immune response genes but not p53-dependent transcription. J Virol. 2009; 83(8):3591-603. doi: 10.1128/JVI.02269-08 PMID: 19211769; PubMed Central PMCID: PMC2663238.
17. Routes JM, Ryan S, Morris K, Takaki R, Cerwenka A, Lanier LL. Adenovirus serotype 5 E1A sensitizes tumor cells to NKG2D-dependent NK cell lysis and tumor rejection. J Exp Med. 2005; 202(11):1477-82. doi: 10.1084/jem.20050240 PMID: 16314433; PubMed Central PMCID: PMC2213342.
18. McSharry BP, Burgert HG, Owen DP, Stanton RJ, Prod'homme V, Sester M, et al. Adenovirus E3/19K promotes evasion of NK cell recognition by intracellular sequestration of the NKG2D ligands major histocompatibility complex class I chain-related proteins A and B. J Virol. 2008; 82(9):4585-94. doi: 10.1128/JVI.02251-07 PMID: 18287244; PubMed Central PMCID: PMCPMC2293069.
19. Champsaur M, Lanier LL. Effect of NKG2D ligand expression on host immune responses. Immunol Rev. 2010; 235(1):267-85. doi: 10.1111/j.0105-2896.2010.00893.x PMID: 20536569; PubMed Central PMCID: PMC2885032.
20. Babiss LE, Ginsberg HS, Darnell JE Jr. Adenovirus E1B proteins are required for accumulation of late viral mRNA and for effects on cellular mRNA translation and transport. Mol Cell Biol. 1985; 5(10):2552-8. PMID: 2942759; PubMed Central PMCID: PMC366989.
21. Goodrum FD, Ornelles DA. Roles for the E4 orf6, orf3, and E1B 55-kilodalton proteins in cell cycle-independent adenovirus replication. J Virol. 1999; 73(9):7474-88. PMID: 10438837; PubMed Central PMCID: PMC104274.
22. Thomas MA, Broughton RS, Goodrum FD, Ornelles DA. E4orf1 limits the oncolytic potential of the E1B-55K deletion mutant adenovirus. J Virol. 2009; 83(6):2406-16. PMID: 19129452. doi: 10.1128/JVI.01972-08
23. Barker DD, Berk AJ. Adenovirus proteins from both E1B reading frames are required for transformation of rodent cells by viral infection and DNA transfection. Virology. 1987; 156(1):107-21. PMID: 2949421.
24. Coutelier JP, van der Logt JT, Heessen FW, Warnier G, Van Snick J. IgG2a restriction of murine antibodies elicited by viral infections. J Exp Med. 1987; 165(1):64-9. PMID: 3794607; PubMed Central PMCID: PMC2188250.
25. Bett AJ, Prevec L, Graham FL. Packaging capacity and stability of human adenovirus type 5 vectors. J Virol. 1993; 67(10):5911-21. PMID: 8371349; PubMed Central PMCID: PMC238011.
26. Qiu F, Bi S, Wang Y, Guo M, Yi Y, Chen S, et al. Hepatitis C virus-specific cellular and humoral immune responses following immunization with a multi-epitope fusion protein. Int J Mol Med. 2012; 29(1):12-7. doi: 10.3892/ijmm.2011.801 PMID: 21956746.
27. Tanghe A, D'Souza S, Rosseels V, Denis O, Ottenhoff TH, Dalemans W, et al. Improved immunogenicity and protective efficacy of a tuberculosis DNA vaccine encoding Ag85 by protein boosting. Infect Immun. 2001; 69(5):3041-7. doi: 10.1128/IAI.69.5.3041-3047.2001 PMID: 11292722; PubMed Central PMCID: PMC98258.
28. Schaack J, Bennett ML, Colbert JD, Torres AV, Clayton GH, Ornelles D, et al. E1A and E1B proteins inhibit inflammation induced by adenovirus. Proc Natl Acad Sci U S A. 2004; 101(9):3124-9. doi: 10.1073/pnas.0303709101 PMID: 14976240; PubMed Central PMCID: PMC365754.
29. Dutt S, Baker J, Kohrt HE, Kambham N, Sanyal M, Negrin RS, et al. CD8+CD44(hi) but not CD4+CD44 (hi) memory T cells mediate potent graft antilymphoma activity without GVHD. Blood. 2011; 117(11):3230-9. doi: 10.1182/blood-2010-10-312751 PMID: 21239702; PubMed Central PMCID: PMC3062320.