Poxviral promoters for improving the immunogenicity of MVA delivered vaccines

References

• Hochstein-Mintzel V, Huber HC, Stickl H. [Virulence and immunogenicity of a modified vaccinia virus (strain MVA) (author’s transl)]. Z Immunitatsforsch Exp Klin Immunol. 1972;144(2):104–156.
   PubMedGoogle Scholar
• Mayr A, Stickl H, Müller HK, Danner K, Singer H. [The smallpox vaccination strain MVA: marker, genetic structure, experience gained with the parenteral vaccination and behavior in organisms with a debilitated defence mechanism (author’s transl)]. Zentralbl Bakteriol B. 1978;167(5–6):375–390.
   PubMedGoogle Scholar
• Sutter G, Staib C. Vaccinia vectors as candidate vaccines: the development of modified vaccinia virus Ankara for antigen delivery. Curr Drug Targets Infect Disord. 2003;3(3):263–271.
   PubMedGoogle Scholar
• Gomez CE, Perdiguero B, Garcia-Arriaza J, Esteban M. Poxvirus vectors as HIV/AIDS vaccines in humans. Hum Vaccin Immunother. 2012;8(9):1192–1207. doi:10.4161/hv.20778.
   PubMed Web of Science ®Google Scholar
• Gilbert SC. Clinical development of Modified Vaccinia virus Ankara vaccines. Vaccine. 2013;31(39):4241–4246. doi:10.1016/j.vaccine.2013.03.020.
   PubMed Web of Science ®Google Scholar
• Volz A, Sutter G. Protective efficacy of Modified Vaccinia virus Ankara in preclinical studies. Vaccine. 2013;31(39):4235–4240. doi:10.1016/j.vaccine.2013.03.016.
   PubMed Web of Science ®Google Scholar
• Volz A, Kupke A, Song F, Jany S, Fux R, Shams-Eldin H, Schmidt J, Becker C, Eickmann M, Becker S, et al. Protective efficacy of recombinant Modified Vaccinia virus Ankara (MVA) delivering Middle East Respiratory Syndrome coronavirus spike glycoprotein. J Virol. 2015. doi:10.1128/JVI.00614-15.
   PubMedGoogle Scholar
• Stanley DA, Honko AN, Asiedu C, Trefry JC, Lau-Kilby AW, Johnson JC, Hensley L, Ammendola V, Abbate A, Grazioli F, et al. Chimpanzee adenovirus vaccine generates acute and durable protective immunity against ebolavirus challenge. Nat Med. 2014;20(10):1126–1129. doi:10.1038/nm.3702.
   PubMed Web of Science ®Google Scholar
• Hill AV, Reyes-Sandoval A, O’Hara G, Ewer K, Lawrie A, Goodman A, Nicosia A, Folgori A, Colloca S, Cortese R, et al. Prime-boost vectored malaria vaccines: progress and prospects. Hum Vaccin. 2010;6(1):78–83.
   PubMed Web of Science ®Google Scholar
• Gilbert SC, Moorthy VS, Andrews L, Pathan AA, McConkey SJ, Vuola JM, Keating SM, Berthoud T, Webster D, McShane H, et al. Synergistic DNA-MVA prime-boost vaccination regimes for malaria and tuberculosis. Vaccine. 2006;24(21):4554–4561. doi:10.1016/j.vaccine.2005.08.048.
   PubMed Web of Science ®Google Scholar
• Acres B, Bonnefoy JY. Clinical development of MVA-based therapeutic cancer vaccines. Expert Rev Vaccines. 2008;7(7):889–893. doi:10.1586/14760584.7.7.889.
   PubMed Web of Science ®Google Scholar
• Garcia-Arriaza J, Esteban M. Enhancing poxvirus vectors vaccine immunogenicity. Hum Vaccin Immunother. 2014;10(8):2235–2244. doi:10.4161/hv.28974.
   PubMed Web of Science ®Google Scholar
• Wyatt LS, Shors ST, Murphy BR, Moss B. Development of a replication-deficient recombinant vaccinia virus vaccine effective against parainfluenza virus 3 infection in an animal model. Vaccine. 1996;14(15):1451–1458.
   PubMed Web of Science ®Google Scholar
• Chakrabarti S, Sisler JR, Moss B. Compact, synthetic, vaccinia virus early/late promoter for protein expression. Biotechniques. 1997;23(6):1094–1097.
   PubMed Web of Science ®Google Scholar
• Hammond JM, Oke PG, Coupar BE. A synthetic vaccinia virus promoter with enhanced early and late activity. J Virol Methods. 1997;66(1):135–138.
   PubMed Web of Science ®Google Scholar
• Orubu T, Alharbi NK, Lambe T, Gilbert SC, Cottingham MG, Verhasselt B. Expression and cellular immunogenicity of a transgenic antigen driven by endogenous poxviral early promoters at their authentic loci in MVA. PLoS One. 2012;7(6):e40167. doi:10.1371/journal.pone.0040167.
   PubMed Web of Science ®Google Scholar
• Venkatesan S, Baroudy BM, Moss B. Distinctive nucleotide sequences adjacent to multiple initiation and termination sites of an early vaccinia virus gene. Cell. 1981;25(3):805–813.
   PubMed Web of Science ®Google Scholar
• Broyles SS. Vaccinia virus transcription. J Gen Virol. 2003;84(Pt 9):2293–2303. doi:10.1099/vir.0.18942-0.
   PubMedGoogle Scholar
• Miner JN, Tamin A, Hruby DE. Anchoring a vaccinia virus promoter in the nucleus prevents its trans-activation by viral infection. Virus Genes. 1990;3(4):355–359.
   PubMedGoogle Scholar
• Assarsson E, Greenbaum JA, Sundström M, Schaffer L, Hammond JA, Pasquetto V, Oseroff C, Hendrickson RC, Lefkowitz EJ, Tscharke DC, et al. Kinetic analysis of a complete poxvirus transcriptome reveals an immediate-early class of genes. Proc Natl Acad Sci USA. 2008;105(6):2140–2145. doi:10.1073/pnas.0711573105.
   PubMed Web of Science ®Google Scholar
• Yang Z, Bruno DP, Martens CA, Porcella SF, Moss B. Simultaneous high-resolution analysis of vaccinia virus and host cell transcriptomes by deep RNA sequencing. Proc Natl Acad Sci USA. 2010;107(25):11513–11518. doi:10.1073/pnas.1006594107.
   PubMed Web of Science ®Google Scholar
• Rubins KH, Hensley LE, Bell GW, Wang C, Lefkowitz EJ, Brown PO, Relman DA, Califano A. Comparative analysis of viral gene expression programs during poxvirus infection: a transcriptional map of the vaccinia and monkeypox genomes. PLoS One. 2008;3(7):e2628. doi:10.1371/journal.pone.0002628.
   PubMed Web of Science ®Google Scholar
• Yang Z, Bruno DP, Martens CA, Porcella SF, Moss B. Genome-wide analysis of the 5ʹ and 3ʹ ends of vaccinia virus early mRNAs delineates regulatory sequences of annotated and anomalous transcripts. J Virol. 2011;85(12):5897–5909. doi:10.1128/JVI.00428-11.
   PubMed Web of Science ®Google Scholar
• Sancho MC, Schleich S, Griffiths G, Krijnse-Locker J. The block in assembly of modified vaccinia virus Ankara in HeLa cells reveals new insights into vaccinia virus morphogenesis. J Virol. 2002;76(16):8318–8334.
   PubMed Web of Science ®Google Scholar
• Geiben-Lynn R, Greenland JR, Frimpong-Boateng K, Letvin NL. Kinetics of recombinant adenovirus type 5, vaccinia virus, modified vaccinia ankara virus, and DNA antigen expression in vivo and the induction of memory T-lymphocyte responses. Clin Vaccine Immunol. 2008;15(4):691–696. doi:10.1128/CVI.00418-07.
   PubMed Web of Science ®Google Scholar
• Prideaux CT, Kumar S, Boyle DB. Comparative analysis of vaccinia virus promoter activity in fowlpox and vaccinia virus recombinants. Virus Res. 1990;16(1):43–57.
   PubMed Web of Science ®Google Scholar
• Tripathy DN, Wittek R. Regulation of foreign gene in fowlpox virus by a vaccinia virus promoter. Avian Dis. 1990;34(1):218–220.
   PubMed Web of Science ®Google Scholar
• Binns MM, Boursnell ME, Tomley FM, Campbell J. Analysis of the fowlpoxvirus gene encoding the 4b core polypeptide and demonstration that it possesses efficient promoter sequences. Virology. 1989;170(1):288–291.
   PubMed Web of Science ®Google Scholar
• Funahashi S, Sato T, Shida H. Cloning and characterization of the gene encoding the major protein of the A-type inclusion body of cowpox virus. J Gen Virol. 1988;69(Pt 1):35–47. doi:10.1099/0022-1317-69-1-35.
   PubMedGoogle Scholar
• Zhang L, Jin N, Song Y, Wang H, Ma H, Li Z, Jiang W. Construction and characterization of a recombinant fowlpox virus containing HIV-1 multi-epitope-p24 chimeric gene in mice. Sci China C Life Sci. 2007;50(2):212–220. doi:10.1007/s11427-007-0017-1.
   PubMedGoogle Scholar
• Timm A, Enzinger C, Felder E, Chaplin P. Genetic stability of recombinant MVA-BN. Vaccine. 2006;24(21):4618–4621. doi:10.1016/j.vaccine.2005.08.037.
   PubMed Web of Science ®Google Scholar
• Kumar S, Boyle DB. Activity of a fowlpox virus late gene promoter in vaccinia and fowlpox virus recombinants. Arch Virol. 1990;112(3–4):139–148.
   PubMed Web of Science ®Google Scholar
• Hopkins R, Bridgeman A, Joseph J, Gilbert SC, McShane H, Hanke T, Zhang L. Dual neonate vaccine platform against HIV-1 and M. tuberculosis. PLoS One. 2011;6(5):e20067. doi:10.1371/journal.pone.0020067.
   PubMed Web of Science ®Google Scholar
• Wyatt LS, Earl PL, Vogt J, Eller LA, Chandran D, Liu J, Robinson HL, Moss B. Correlation of immunogenicities and in vitro expression levels of recombinant modified vaccinia virus Ankara HIV vaccines. Vaccine. 2008;26(4):486–493. doi:10.1016/j.vaccine.2007.11.036.
   PubMed Web of Science ®Google Scholar
• Di Pilato M, Mejías-Pérez E, Gómez CE, Perdiguero B, Sorzano COS, Esteban M. New vaccinia virus promoter as a potential candidate for future vaccines. J Gen Virol. 2013;94(Pt 12):2771–2776. doi:10.1099/vir.0.057299-0.
   PubMedGoogle Scholar
• Mackett M, Smith GL. Vaccinia virus expression vectors. J Gen Virol. 1986;67(Pt 10):2067–2082. doi:10.1099/0022-1317-67-10-2067.
   PubMedGoogle Scholar
• Wittek R, Hanggi M, Hiller G. Mapping of a gene coding for a major late structural polypeptide on the vaccinia virus genome. J Virol. 1984;49(2):371–378.
   PubMed Web of Science ®Google Scholar
• Antoine G, Scheiflinger F, Dorner F, Falkner FG. The complete genomic sequence of the modified vaccinia Ankara strain: comparison with other orthopoxviruses. Virology. 1998;244(2):365–396. doi:10.1006/viro.1998.9123.
   PubMed Web of Science ®Google Scholar
• Schmitt JF, Stunnenberg HG. Sequence and transcriptional analysis of the vaccinia virus HindIII I fragment. J Virol. 1988;62(6):1889–1897.
   PubMed Web of Science ®Google Scholar
• Liu X, Kremer M, Broyles SS. A natural vaccinia virus promoter with exceptional capacity to direct protein synthesis. J Virol Methods. 2004;122(2):141–145. doi:10.1016/j.jviromet.2004.08.009.
   PubMed Web of Science ®Google Scholar
• Cochran MA, Puckett C, Moss B. In vitro mutagenesis of the promoter region for a vaccinia virus gene: evidence for tandem early and late regulatory signals. J Virol. 1985;54(1):30–37.
   PubMed Web of Science ®Google Scholar
• Weir JP, Moss B. Determination of the promoter region of an early vaccinia virus gene encoding thymidine kinase. Virology. 1987;158(1):206–210.
   PubMed Web of Science ®Google Scholar
• Coupar BE, Boyle DB, Both GW. Effect of in vitro mutations in a vaccinia virus early promoter region monitored by herpes simplex virus thymidine kinase expression in recombinant vaccinia virus. J Gen Virol. 1987;68(Pt 9):2299–2309. doi:10.1099/0022-1317-68-9-2299.
   PubMedGoogle Scholar
• Perkus ME, Limbach K, Paoletti E. Cloning and expression of foreign genes in vaccinia virus, using a host range selection system. J Virol. 1989;63(9):3829–3836.
   PubMed Web of Science ®Google Scholar
• Rosel JL, Earl PL, Weir JP, Moss B. Conserved TAAATG sequence at the transcriptional and translational initiation sites of vaccinia virus late genes deduced by structural and functional analysis of the HindIII H genome fragment. J Virol. 1986;60(2):436–449.
   PubMed Web of Science ®Google Scholar
• Baur K, Brinkmann K, Schweneker M, Pätzold J, Meisinger-Henschel C, Hermann J, Steigerwald R, Chaplin P, Suter M, Hausmann J. Immediate-early expression of a recombinant antigen by modified vaccinia virus ankara breaks the immunodominance of strong vector-specific B8R antigen in acute and memory CD8 T-cell responses. J Virol. 2010;84(17):8743–8752. doi:10.1128/JVI.00604-10.
   PubMed Web of Science ®Google Scholar
• Garces J, Masternak K, Kunz B, Wittek R. Reactivation of transcription from a vaccinia virus early promoter late in infection. J Virol. 1993;67(9):5394–5401.
   PubMed Web of Science ®Google Scholar
• Panicali D, Paoletti E. Construction of poxviruses as cloning vectors: insertion of the thymidine kinase gene from herpes simplex virus into the DNA of infectious vaccinia virus. Proc Natl Acad Sci USA. 1982;79(16):4927–4931.
   PubMed Web of Science ®Google Scholar
• Perkus ME, Piccini A, Lipinskas BR, Paoletti E. Recombinant vaccinia virus: immunization against multiple pathogens. Science. 1985;229(4717):981–984.
   PubMed Web of Science ®Google Scholar
• Alharbi NK, Spencer AJ, Salman AM, Tully CM, Chinnakannan SK, Lambe T, Yamaguchi Y, Morris SJ, Orubu T, Draper SJ, et al. Enhancing cellular immunogenicity of MVA-vectored vaccines by utilizing the F11L endogenous promoter. Vaccine. 2016;34(1):49–55. doi:10.1016/j.vaccine.2015.11.028.
   PubMed Web of Science ®Google Scholar
• Wennier ST, Brinkmann K, Steinhäußer C, Mayländer N, Mnich C, Wielert U, Dirmeier U, Hausmann J, Chaplin P, Steigerwald R, et al. A novel naturally occurring tandem promoter in modified vaccinia virus ankara drives very early gene expression and potent immune responses. PLoS One. 2013;8(8):e73511. doi:10.1371/journal.pone.0073511.
   PubMed Web of Science ®Google Scholar
• Davison AJ, Moss B. Structure of vaccinia virus early promoters. J Mol Biol. 1989;210(4):749–769.
   PubMed Web of Science ®Google Scholar
• Davison AJ, Moss B. Structure of vaccinia virus late promoters. J Mol Biol. 1989;210(4):771–784.
   PubMed Web of Science ®Google Scholar
• Hirschmann P, Vos JC, Stunnenberg HG. Mutational analysis of a vaccinia virus intermediate promoter in vivo and in vitro. J Virol. 1990;64(12):6063–6069.
   PubMed Web of Science ®Google Scholar
• Di Pilato M, Sánchez-Sampedro L, Mejías-Pérez E, Di Pilato M, Esteban M. Modification of promoter spacer length in vaccinia virus as a strategy to control the antigen expression. J Gen Virol. 2015. doi:10.1099/vir.0.000183.
   PubMed Web of Science ®Google Scholar
• Alharbi NK, Chinnakannan SK, Gilbert SC, Draper SJ, Jan E. Investigation of IRES insertion into the genome of recombinant MVA as a translation enhancer in the context of transcript decapping. PLoS One. 2015;10(5):e0127978. doi:10.1371/journal.pone.0127978.
   PubMed Web of Science ®Google Scholar
• Ramirez JC, Gherardi MM, Esteban M. Biology of attenuated modified vaccinia virus Ankara recombinant vector in mice: virus fate and activation of B- and T-cell immune responses in comparison with the Western Reserve strain and advantages as a vaccine. J Virol. 2000;74(2):923–933.
   PubMed Web of Science ®Google Scholar
• Wang Z, Martinez J, Zhou W, La Rosa C, Srivastava T, Dasgupta A, Rawal R, Li Z, Britt WJ, Diamond D. Modified H5 promoter improves stability of insert genes while maintaining immunogenicity during extended passage of genetically engineered MVA vaccines. Vaccine. 2010;28(6):1547–1557. doi:10.1016/j.vaccine.2009.11.056.
   PubMed Web of Science ®Google Scholar
• Coupar BE, Andrew ME, Both GW, Boyle DB. Temporal regulation of influenza hemagglutinin expression in vaccinia virus recombinants and effects on the immune response. Eur J Immunol. 1986;16(12):1479–1487. doi:10.1002/eji.1830161203.
   PubMed Web of Science ®Google Scholar
• Bronte V, Carroll MW, Goletz TJ, Wang M, Overwijk WW, Marincola F, Rosenberg SA, Moss B, Restifo NP. Antigen expression by dendritic cells correlates with the therapeutic effectiveness of a model recombinant poxvirus tumor vaccine. Proc Natl Acad Sci USA. 1997;94(7):3183–3188.
   PubMed Web of Science ®Google Scholar
• Oseroff C, Kos F, Bui -H-H, Peters B, Pasquetto V, Glenn J, Palmore T, Sidney J, Tscharke DC, Bennink JR, et al. HLA class I-restricted responses to vaccinia recognize a broad array of proteins mainly involved in virulence and viral gene regulation. Proc Natl Acad Sci USA. 2005;102(39):13980–13985. doi:10.1073/pnas.0506768102.
   PubMed Web of Science ®Google Scholar
• Tscharke DC, Karupiah G, Zhou J, Palmore T, Irvine KR, Haeryfar SMM, Williams S, Sidney J, Sette A, Bennink JR, et al. Identification of poxvirus CD8+ T cell determinants to enable rational design and characterization of smallpox vaccines. J Exp Med. 2005;201(1):95–104. doi:10.1084/jem.20041912.
   PubMed Web of Science ®Google Scholar
• Draper SJ, Cottingham MG, Gilbert SC. Utilizing poxviral vectored vaccines for antibody induction-progress and prospects. Vaccine. 2013;31(39):4223–4230. doi:10.1016/j.vaccine.2013.05.091.
   PubMed Web of Science ®Google Scholar
• Davies DH, Wyatt LS, Newman FK, Earl PL, Chun S, Hernandez JE, Molina DM, Hirst S, Moss B, Frey SE, et al. Antibody profiling by proteome microarray reveals the immunogenicity of the attenuated smallpox vaccine modified vaccinia virus ankara is comparable to that of Dryvax. J Virol. 2008;82(2):652–663. doi:10.1128/JVI.01706-07.
   PubMed Web of Science ®Google Scholar
• Garber DA, O’Mara LA, Zhao J, Gangadhara S, An I, Feinberg MB, Sommer P. Expanding the repertoire of Modified Vaccinia Ankara-based vaccine vectors via genetic complementation strategies. PLoS One. 2009;4(5):e5445. doi:10.1371/journal.pone.0005445.
   PubMed Web of Science ®Google Scholar
• Alharbi NK. New approaches for improving the immunogenicity of modified vaccinia virus Ankara as a recombinant vaccine vector [ PhD thesis]. Oxford, UK: Oxford University; 2014.
   Google Scholar
• Wyatt LS, Earl PL, Xiao W, Americo JL, Cotter CA, Vogt J, Moss B. Elucidating and minimizing the loss by recombinant vaccinia virus of human immunodeficiency virus gene expression resulting from spontaneous mutations and positive selection. J Virol. 2009;83(14):7176–7184. doi:10.1128/JVI.00687-09.
   PubMed Web of Science ®Google Scholar
• Stittelaar KJ, Wyatt LS, De Swart RL, Vos HW, Groen J, Van Amerongen G, Van Binnendijk RS, Rozenblatt S, Moss B, Osterhaus AD. Protective immunity in macaques vaccinated with a modified vaccinia virus Ankara-based measles virus vaccine in the presence of passively acquired antibodies. J Virol. 2000;74(9):4236–4243.
   PubMed Web of Science ®Google Scholar
• Tameris MD, Hatherill M, Landry BS, Scriba TJ, Snowden MA, Lockhart S, Shea JE, McClain JB, Hussey GD, Hanekom WA, et al. Safety and efficacy of MVA85A, a new tuberculosis vaccine, in infants previously vaccinated with BCG: a randomised, placebo-controlled phase 2b trial. Lancet. 2013;381(9871):1021–1028. doi:10.1016/S0140-6736(13)60177-4.
   PubMed Web of Science ®Google Scholar