A Novel Naturally Occurring Tandem Promoter in Modified Vaccinia Virus Ankara Drives Very Early Gene Expression and Potent Immune Responses

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Wennier, Sonia T ^a   Brinkmann, Kay ^a   Steinhäußer, Charlotte ^a   Mayländer, Nicole ^a   Mnich, Claudia ^a   Wielert, Ursula ^a   Dirmeier, Ulrike ^a   Hausmann, Jürgen ^a   Chaplin, Paul ^a   Steigerwald, Robin ^a  

^a Bavarian Nordic GmbH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

VACCINIA VACCINE; VIRUS VECTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY TITER; ANTIGEN SPECIFICITY; ARTICLE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; EMBRYO; FEMALE; GENE EXPRESSION; IMMUNIZATION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; POXVIRUS; PROMOTER REGION; TANDEM REPEAT; VACCINIA VIRUS; VIRUS GENE; VIRUS GENOME; VIRUS IMMUNITY; VIRUS RECOMBINANT; VIRUS REPLICATION;

ANIMALS; ANTIBODIES, VIRAL; ANTIGENS; BASE SEQUENCE; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE; CHICK EMBRYO; FEMALE; GENE EXPRESSION; GENE ORDER; GENETIC VECTORS; HUMANS; IMMUNITY, CELLULAR; IMMUNITY, HUMORAL; IMMUNOLOGIC MEMORY; MICE; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS, GENETIC; VACCINIA VIRUS; VIRAL VACCINES;

EID: 84881516521     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0073511     Document Type: Article

References (49)

1. Mackett M, Smith GL, Moss B, (1982) Vaccinia virus: a selectable eukaryotic cloning and expression vector. Proc Natl Acad Sci U S A 79: 7415-7419. doi:10.1073/pnas.79.23.7415. PubMed: 6296831.
2. Moss B, (1991) Vaccinia virus: a tool for research and vaccine development. Science 252: 1662-1667. doi:10.1126/science.2047875. PubMed: 2047875.
3. Lane JM, Ruben FL, Neff JM, Millar JD, (1969) Complications of smallpox vaccination, 1968. N Engl J Med 281: 1201-1208. doi:10.1056/NEJM196911272812201. PubMed: 4186802.
4. Lane JM, Ruben FL, Abrutyn E, Millar JD, (1970) Deaths attributable to smallpox vaccination, 1959 to 1966, and 1968. JAMA 212: 441-444. doi:10.1001/jama.1970.03170160031005. PubMed: 4392370.
5. Gómez CE, Nájera JL, Krupa M, Perdiguero B, Esteban M, (2011) MVA and NYVAC as vaccines against emergent infectious diseases and cancer. Curr Gene Ther 11: 189-217. doi:10.2174/156652311795684731. PubMed: 21453284.
6. Mayr A, Munz E, (1964) [Changes in the vaccinia virus through continuing passages in chick embryo fibroblast cultures]. Zentralbl Bakteriol Orig 195: 24-35. PubMed: 5890664.
7. Mayr A, Hochstein-Mintzel V, Stickl H, (1975) Abstammung, Eigenschaften und Verwendung des attenuierten Vaccinia-Stammes MVA. Infection 3: 6-14. doi:10.1007/BF01641272.
8. Carroll MW, Moss B, (1997) Host range and cytopathogenicity of the highly attenuated MVA strain of vaccinia virus: propagation and generation of recombinant viruses in a nonhuman mammalian cell line. Virology 238: 198-211. doi:10.1006/viro.1997.8845. PubMed: 9400593.
9. Drexler I, Heller K, Wahren B, Erfle V, Sutter G, (1998) Highly attenuated modified vaccinia virus Ankara replicates in baby hamster kidney cells, a potential host for virus propagation, but not in various human transformed and primary cells. J Gen Virol 79: 347-352. PubMed: 9472619.
10. Blanchard TJ, Alcami A, Andrea P, Smith GL, (1998) Modified vaccinia virus Ankara undergoes limited replication in human cells and lacks several immunomodulatory proteins: implications for use as a human vaccine. J Gen Virol 79: 1159-1167. PubMed: 9603331.
11. Meisinger-Henschel C, Schmidt M, Lukassen S, Linke B, Krause L, et al. (2007) Genomic sequence of chorioallantois vaccinia virus Ankara, the ancestor of modified vaccinia virus Ankara. J Gen Virol 88: 3249-3259. doi:10.1099/vir.0.83156-0. PubMed: 18024893.
12. Meisinger-Henschel C, Späth M, Lukassen S, Wolferstätter M, Kachelriess H, et al. (2010) Introduction of the six major genomic deletions of modified vaccinia virus Ankara (MVA) into the parental vaccinia virus is not sufficient to reproduce an MVA-like phenotype in cell culture and in mice. J Virol 84: 9907-9919. doi:10.1128/JVI.00756-10. PubMed: 20668072.
13. Kennedy JS, Greenberg RN, (2009) IMVAMUNE: modified vaccinia Ankara strain as an attenuated smallpox vaccine. Expert Rev Vaccines 8: 13-24. doi:10.1586/14760584.8.1.13. PubMed: 19093767.
14. Vollmar J, Arndtz N, Eckl KM, Thomsen T, Petzold B, et al. (2006) Safety and immunogenicity of IMVAMUNE, a promising candidate as a third generation smallpox vaccine. Vaccine 24: 2065-2070. doi:10.1016/j.vaccine.2005.11.022. PubMed: 16337719.
15. von Krempelhuber A, Vollmar J, Pokorny R, Rapp P, Wulff N, et al. (2010) A randomized, double-blind, dose-finding Phase II study to evaluate immunogenicity and safety of the third generation smallpox vaccine candidate IMVAMUNE. Vaccine 28: 1209-1216. doi:10.1016/j.vaccine.2009.11.030. PubMed: 19944151.
16. Greenberg RN, Overton ET, Haas DW, Frank I, Goldman M, et al. (2013) Safety, immunogenicity, and surrogate markers of clinical efficacy for modified vaccinia Ankara as a smallpox vaccine in HIV-infected subjects. J Infect Dis 207: 749-758. doi:10.1093/infdis/jis753. PubMed: 23225902.
17. Funahashi S, Itamura S, Iinuma H, Nerome K, Sugimoto M, et al. (1991) Increased expression in vivo and in vitro of foreign genes directed by A-type inclusion body hybrid promoters in recombinant vaccinia viruses. J Virol 65: 5584-5588. PubMed: 1654453.
18. Wyatt LS, Earl PL, Vogt J, Eller LA, Chandran D, et al. (2008) Correlation of immunogenicities and in vitro expression levels of recombinant modified vaccinia virus Ankara HIV vaccines. Vaccine 26: 486-493. doi:10.1016/j.vaccine.2007.11.036. PubMed: 18155813.
19. Broyles SS, (2003) Vaccinia virus transcription. J Gen Virol 84: 2293-2303. doi:10.1099/vir.0.18942-0. PubMed: 12917449.
20. Moutaftsi M, Tscharke DC, Vaughan K, Koelle DM, Stern L, et al. (2010) Uncovering the interplay between CD8, CD4 and antibody responses to complex pathogens. Future Microbiol 5: 221-239. doi:10.2217/fmb.09.110. PubMed: 20143946.
21. Yang Z, Reynolds SE, Martens CA, Bruno DP, Porcella SF, et al. (2011) Expression profiling of the intermediate and late stages of poxvirus replication. J Virol 85: 9899-9908. doi:10.1128/JVI.05446-11. PubMed: 21795349.
22. Moutaftsi M, Bui HH, Peters B, Sidney J, Salek-Ardakani S, et al. (2007) Vaccinia virus-specific CD4+ T cell responses target a set of antigens largely distinct from those targeted by CD8+ T cell responses. J Immunol 178: 6814-6820. PubMed: 17513729.
23. Baur K, Brinkmann K, Schweneker M, Pätzold J, Meisinger-Henschel C, et al. (2010) 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 84: 8743-8752. doi:10.1128/JVI.00604-10. PubMed: 20538860.
24. Cochran MA, Puckett C, Moss B, (1985) In vitro mutagenesis of the promoter region for a vaccinia virus gene: evidence for tandem early and late regulatory signals. J Virol 54: 30-37. PubMed: 3973982.
25. Wyatt LS, Shors ST, Murphy BR, Moss B, (1996) Development of a replication-deficient recombinant vaccinia virus vaccine effective against parainfluenza virus 3 infection in an animal model. Vaccine 14: 1451-1458. doi:10.1016/S0264-410X(96)00072-2. PubMed: 8994321.
26. Chakrabarti S, Sisler JR, Moss B, (1997) Compact, synthetic, vaccinia virus early/late promoter for protein expression. BioTechniques 23: 1094-1097. PubMed: 9421642.
27. Davison AJ, Moss B, (1989) Structure of vaccinia virus early promoters. J Mol Biol 210: 749-769. doi:10.1016/0022-2836(89)90107-1. PubMed: 2515286.
28. Davison AJ, Moss B, (1989) Structure of vaccinia virus late promoters. J Mol Biol 210: 771-784. doi:10.1016/0022-2836(89)90108-3. PubMed: 2515287.
29. Jin NY, Funahashi S, Shida H, (1994) Constructions of vaccinia virus A-type inclusion body protein, tandemly repeated mutant 7.5 kDa protein, and hemagglutinin gene promoters support high levels of expression. Arch Virol 138: 315-330. doi:10.1007/BF01379134. PubMed: 7998837.
30. Yang Z, Bruno DP, Martens CA, Porcella SF, Moss B, (2010) Simultaneous high-resolution analysis of vaccinia virus and host cell transcriptomes by deep RNA sequencing. Proc Natl Acad Sci U S A 107: 11513-11518. doi:10.1073/pnas.1006594107. PubMed: 20534518.
31. Assarsson E, Greenbaum JA, Sundström M, Schaffer L, Hammond JA, et al. (2008) Kinetic analysis of a complete poxvirus transcriptome reveals an immediate-early class of genes. Proc Natl Acad Sci U S A 105: 2140-2145. doi:10.1073/pnas.0711573105. PubMed: 18245380.
32. Orubu T, Alharbi NK, Lambe T, Gilbert SC, Cottingham MG, (2012) Expression and cellular immunogenicity of a transgenic antigen driven by endogenous poxviral early promoters at their authentic loci in MVA. PLOS ONE 7: e40167. doi:10.1371/journal.pone.0040167. PubMed: 22761956.
33. Yang Z, Bruno DP, Martens CA, Porcella SF, Moss B, (2011) Genome-wide analysis of the 5' and 3' ends of vaccinia virus early mRNAs delineates regulatory sequences of annotated and anomalous transcripts. J Virol 85: 5897-5909. doi:10.1128/JVI.00428-11. PubMed: 21490097.
34. Schweneker M, Lukassen S, Späth M, Wolferstätter M, Babel E, et al. (2012) The vaccinia virus O1 protein is required for sustained activation of extracellular signal-regulated kinase 1/2 and promotes viral virulence. J Virol 86: 2323-2336. doi:10.1128/JVI.06166-11. PubMed: 22171261.
35. Sancho MC, Schleich S, Griffiths G, Krijnse-Locker J, (2002) The block in assembly of modified vaccinia virus Ankara in HeLa cells reveals new insights into vaccinia virus morphogenesis. J Virol 76: 8318-8334. doi:10.1128/JVI.76.16.8318-8334.2002. PubMed: 12134037.
36. Hruby DE, Lynn DL, Condit RC, Kates JR, (1980) Cellular differences in the molecular mechanisms of vaccinia virus host range restriction. J Gen Virol 47: 485-488. doi:10.1099/0022-1317-47-2-485. PubMed: 6767809.
37. Frey SE, Newman FK, Kennedy JS, Sobek V, Ennis FA, et al. (2007) Clinical and immunologic responses to multiple doses of IMVAMUNE (Modified Vaccinia Ankara) followed by Dryvax challenge. Vaccine 25: 8562-8573. doi:10.1016/j.vaccine.2007.10.017. PubMed: 18036708.
38. Wyatt LS, Earl PL, Eller LA, Moss B, (2004) Highly attenuated smallpox vaccine protects mice with and without immune deficiencies against pathogenic vaccinia virus challenge. Proc Natl Acad Sci U S A 101: 4590-4595. doi:10.1073/pnas.0401165101. PubMed: 15070762.
39. Broyles SS, Li J, Moss B, (1991) Promoter DNA contacts made by the vaccinia virus early transcription factor. J Biol Chem 266: 15539-15544. PubMed: 1869571.
40. Cassetti MA, Moss B, (1996) Interaction of the 82-kDa subunit of the vaccinia virus early transcription factor heterodimer with the promoter core sequence directs downstream DNA binding of the 70-kDa subunit. Proc Natl Acad Sci U S A 93: 7540-7545. doi:10.1073/pnas.93.15.7540. PubMed: 8755510.
41. Moutaftsi M, Peters B, Pasquetto V, Tscharke DC, Sidney J, et al. (2006) A consensus epitope prediction approach identifies the breadth of murine T(CD8+)-cell responses to vaccinia virus. Nat Biotechnol 24: 817-819. doi:10.1038/nbt1215. PubMed: 16767078.
42. Tscharke DC, Woo WP, Sakala IG, Sidney J, Sette A, et al. (2006) Poxvirus CD8+ T-cell determinants and cross-reactivity in BALB/c mice. J Virol 80: 6318-6323. doi:10.1128/JVI.00427-06. PubMed: 16775319.
43. Sette A, Grey H, Oseroff C, Peters B, Moutaftsi M, et al. (2009) Definition of epitopes and antigens recognized by vaccinia specific immune responses: their conservation in variola virus sequences, and use as a model system to study complex pathogens. Vaccine 27 (Suppl 6):: G21-G26. doi:10.1016/j.vaccine.2009.10.011. PubMed: 20006135.
44. Walsh SR, Gillis J, Peters B, Mothé BR, Sidney J, et al. (2009) Diverse recognition of conserved orthopoxvirus CD8+ T cell epitopes in vaccinated rhesus macaques. Vaccine 27: 4990-5000. doi:10.1016/j.vaccine.2009.05.077. PubMed: 19531389.
45. Oseroff C, Peters B, Pasquetto V, Moutaftsi M, Sidney J, et al. (2008) Dissociation between epitope hierarchy and immunoprevalence in CD8 responses to vaccinia virus western reserve. J Immunol 180: 7193-7202. PubMed: 18490718.
46. Kastenmuller W, Gasteiger G, Gronau JH, Baier R, Ljapoci R, et al. (2007) Cross-competition of CD8+ T cells shapes the immunodominance hierarchy during boost vaccination. J Exp Med 204: 2187-2198. doi:10.1084/jem.20070489. PubMed: 17709425.
47. Wilck MB, Seaman MS, Baden LR, Walsh SR, Grandpre LE, et al. (2010) Safety and immunogenicity of modified vaccinia Ankara (ACAM3000): effect of dose and route of administration. J Infect Dis 201: 1361-1370. doi:10.1086/651561. PubMed: 20350191.
48. Tscharke DC, Karupiah G, Zhou J, Palmore T, Irvine KR, et al. (2005) Identification of poxvirus CD8+ T cell determinants to enable rational design and characterization of smallpox vaccines. J Exp Med 201: 95-104. doi:10.1084/jem.20041912. PubMed: 15623576.
49. Howley PM, Spehner D, Drillien R, (1996) A vaccinia virus transfer vector using a GUS reporter gene inserted into the I4L locus. Gene 172: 233-237. doi:10.1016/0378-1119(96)00192-8. PubMed: 8682309.