1887

Abstract

Since 1980 there has been global eradication of smallpox due to the success of the vaccination programme using vaccinia virus (VACV). During the eradication period, distinct VACV strains circulated, the Lister strain being the most commonly employed in Europe. Analysis of the safety of smallpox vaccines has suggested that they display significant heterogeneity. To gain a more detailed understanding of the diversity of VACV strains it is important to determine their genomic sequences. Although the sequences of three isolates of the Japanese Lister original strain (VACV-LO) are available, no analysis of the relationship of any Lister sequence compared to other VACV genomes has been reported. Here, we describe the sequence of a representative clonal isolate of the Lister vaccine (VACV-List) used to inoculate the French population. The coding capacity of VACV-List was compared to other VACV strains. The 201 open reading frames (ORFs) were annotated in the VACV-List genome based on protein size, genomic localization and prior characterization of many ORFs. Eleven ORFs were recognized as pseudogenes as they were truncated or fragmented counterparts of larger ORFs in other orthopoxviruses (OPVs). The VACV-List genome also contains several ORFs that have not been annotated in other VACVs but were found in other OPVs. VACV-List and VACV-LO displayed a high level of nucleotide sequence similarity. Compared to the Copenhagen strain of VACV, the VACV-List sequence diverged in three main regions, one of them corresponding to a substitution in VACV-List with coxpox virus GRI-90 strain ORFs, suggestive of prior genetic exchanges. These studies highlight the heterogeneity between VACV strains and provide a basis to better understand differences in safety and efficacy of smallpox vaccines.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.82708-0
2007-07-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/jgv/88/7/1906.html?itemId=/content/journal/jgv/10.1099/vir.0.82708-0&mimeType=html&fmt=ahah

References

  1. Afonso C. L., Tulman E. R., Lu Z., Zsak L., Sandybaev N. T., Kerembekova U. Z., Zaitsev V. L., Kutish G. F., Rock D. L. 2002; The genome of camelpox virus. Virology 295:1–9 [CrossRef]
    [Google Scholar]
  2. Afonso C. L., Delhon G., Tulman E. R., Lu Z., Zsak A., Becerra V. M., Zsak L., Kutish G. F., Rock D. L. 2005; Genome of deerpox virus. J Virol 79:966–977 [CrossRef]
    [Google Scholar]
  3. Alcami A., Smith G. L. 1995; Vaccinia, cowpox, and camelpox viruses encode soluble gamma interferon receptors with novel broad species specificity. J Virol 69:4633–4639
    [Google Scholar]
  4. Alcami A., Symons J. A., Smith G. L. 2000; The vaccinia virus soluble alpha/beta interferon (IFN) receptor binds to the cell surface and protects cells from the antiviral effects of IFN. J Virol 74:11230–11239 [CrossRef]
    [Google Scholar]
  5. Alejo A., Ruiz-Arguello M. B., Ho Y., Smith V. P., Saraiva M., Alcami A. 2006; A chemokine-binding domain in the tumor necrosis factor receptor from variola (smallpox) virus. Proc Natl Acad Sci U S A 103:5995–6000 [CrossRef]
    [Google Scholar]
  6. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. 1990; Basic local alignment search tool. J Mol Biol 215:403–410 [CrossRef]
    [Google Scholar]
  7. Amegadzie B. Y., Ahn B. Y., Moss B. 1992; Characterization of a 7-kilodalton subunit of vaccinia virus DNA-dependent RNA polymerase with structural similarities to the smallest subunit of eukaryotic RNA polymerase II. J Virol 66:3003–3010
    [Google Scholar]
  8. Antoine G., Scheiflinger F., Dorner F., Falkner F. G. 1998; The complete genomic sequence of the modified vaccinia Ankara strain: comparison with other orthopoxviruses. Virology 244:365–396 [CrossRef]
    [Google Scholar]
  9. Breman J. G., Arita I. 1980; The confirmation and maintenance of smallpox eradication. N Engl J Med 303:1263–1273 [CrossRef]
    [Google Scholar]
  10. Chalifa-Caspi V., Shmueli O., Benjamin-Rodrig H., Rosen N., Shmoish M., Yanai I., Ophir R., Kats P., Safran M., Lancet D. 2003; GeneAnnot: interfacing GeneCards with high-throughput gene expression compendia. Brief Bioinform 4:349–360 [CrossRef]
    [Google Scholar]
  11. Chalifa-Caspi V., Yanai I., Ophir R., Rosen N., Shmoish M., Benjamin-Rodrig H., Shklar M., Stein T. I., Shmueli O. other authors 2004; GeneAnnot: comprehensive two-way linking between oligonucleotide array probesets and GeneCards genes. Bioinformatics 20:1457–1458 [CrossRef]
    [Google Scholar]
  12. Chen N., Danila M. I., Feng Z., Buller R. M., Wang C., Han X., Lefkowitz E. J., Upton C. 2003; The genomic sequence of ectromelia virus, the causative agent of mousepox. Virology 317:165–186 [CrossRef]
    [Google Scholar]
  13. Chung C. S., Chen C. H., Ho M. Y., Huang C. Y., Liao C. L., Chang W. 2006; Vaccinia virus proteome: identification of proteins in vaccinia virus intracellular mature virion particles. J Virol 80:2127–2140 [CrossRef]
    [Google Scholar]
  14. de Carlos A., Paez E. 1991; Isolation and characterization of mutants of vaccinia virus with a modified 94-kDa inclusion protein. Virology 185:768–778 [CrossRef]
    [Google Scholar]
  15. DiPerna G., Stack J., Bowie A. G., Boyd A., Kotwal G., Zhang Z., Arvikar S., Latz E., Fitzgerald K. A., Marshall W. L. 2004; Poxvirus protein N1L targets the I-kappaB kinase complex, inhibits signaling to NF- κ B by the tumor necrosis factor superfamily of receptors, and inhibits NF- κ B and IRF3 signaling by toll-like receptors. J Biol Chem 279:36570–36578 [CrossRef]
    [Google Scholar]
  16. Fenner F. 1982; A successful eradication campaign. Global eradication of smallpox. Rev Infect Dis 4:916–930 [CrossRef]
    [Google Scholar]
  17. Galtier N., Gouy M., Gautier C. 1996; SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci 12:543–548
    [Google Scholar]
  18. Geshelin P., Berns K. I. 1974; Characterization and localization of the naturally occurring cross-links in vaccinia virus DNA. J Mol Biol 88:785–796 [CrossRef]
    [Google Scholar]
  19. Goebel S. J., Johnson G. P., Perkus M. E., Davis S. W., Winslow J. P., Paoletti E. 1990; The complete DNA sequence of vaccinia virus. Virology 179:247–266. 517–563
    [Google Scholar]
  20. Grosenbach D. W., Hansen S. G., Hruby D. E. 2000; Identification and analysis of vaccinia virus palmitylproteins. Virology 275:193–206 [CrossRef]
    [Google Scholar]
  21. Gubser C., Smith G. L. 2002; The sequence of camelpox virus shows it is most closely related to variola virus, the cause of smallpox. J Gen Virol 83:855–872
    [Google Scholar]
  22. Gubser C., Hue S., Kellam P., Smith G. L. 2004; Poxvirus genomes: a phylogenetic analysis. J Gen Virol 85:105–117 [CrossRef]
    [Google Scholar]
  23. Gubser C., Bergamaschi D., Hollinshead M., Lu X., van Kuppeveld F. J., Smith G. L. 2007; A new inhibitor of apoptosis from vaccinia virus and eukaryotes. PloS Pathog 3:e17 [CrossRef]
    [Google Scholar]
  24. Henderson D. A. 1999a; The looming threat of bioterrorism. Science 283:1279–1282 [CrossRef]
    [Google Scholar]
  25. Henderson D. A. 1999b; Weapons for the future. Lancet 354:SIV64 [CrossRef]
    [Google Scholar]
  26. Herrero-Martinez E., Roberts K. L., Hollinshead M., Smith G. L. 2005; Vaccinia virus intracellular enveloped virions move to the cell periphery on microtubules in the absence of the A36R protein. J Gen Virol 86:2961–2968 [CrossRef]
    [Google Scholar]
  27. Huang J., Huang Q., Zhou X., Shen M. M., Yen A., Yu S. X., Dong G., Qu K., Huang P. other authors 2004; The poxvirus p28 virulence factor Is an E3 Ubiquitin ligase. J Biol Chem 279:54110–54116 [CrossRef]
    [Google Scholar]
  28. Kahmann J. D., Wecking D. A., Putter V., Lowenhaupt K., Kim Y. G., Schmieder P., Oschkinat H., Rich A., Schade M. 2004; The solution structure of the N-terminal domain of E3L shows a tyrosine conformation that may explain its reduced affinity to Z-DNA in vitro . Proc Natl Acad Sci U S A 101:2712–2717 [CrossRef]
    [Google Scholar]
  29. Kettle S., Blake N. W., Law K. M., Smith G. L. 1995; Vaccinia virus serpins B13R (SPI-2) and B22R (SPI-1) encode M(r) 38.5 and 40K, intracellular polypeptides that do not affect virus virulence in a murine intranasal model. Virology 206:136–147 [CrossRef]
    [Google Scholar]
  30. Kettle S., Alcami A., Khanna A., Ehret R., Jassoy C., Smith G. L. 1997; Vaccinia virus serpin B13R (SPI-2) inhibits interleukin-1 β -converting enzyme and protects virus-infected cells from TNF- and Fas-mediated apoptosis, but does not prevent IL-1 β -induced fever. J Gen Virol 78:677–685
    [Google Scholar]
  31. Kretzschmar M., Wallinga J., Teunis P., Xing S., Mikolajczyk R. 2006; Frequency of adverse events after vaccination with different vaccinia strains. PLoS Med 3:e272 [CrossRef]
    [Google Scholar]
  32. Langland J. O., Jacobs B. L. 2002; The role of the PKR-inhibitory genes, E3L and K3L, in determining vaccinia virus host range. Virology 299:133–141 [CrossRef]
    [Google Scholar]
  33. Lee L. G., Spurgeon S. L., Heiner C. R., Benson S. C., Rosenblum B. B., Menchen S. M., Graham R. J., Constantinescu A., Upadhya K. G., Cassel J. M. 1997; New energy transfer dyes for DNA sequencing. Nucleic Acids Res 25:2816–2822 [CrossRef]
    [Google Scholar]
  34. Lee H. J., Essani K., Smith G. L. 2001; The genome sequence of Yaba-like disease virus, a yatapoxvirus. Virology 281:170–192 [CrossRef]
    [Google Scholar]
  35. Levy-Bruhl D., Guerin N. 2001; The use of smallpox virus as a biological weapon: the vaccination situation in France. Euro Surveill 6:171–178
    [Google Scholar]
  36. Li G., Chen N., Roper R. L., Feng Z., Hunter A., Danila M., Lefkowitz E. J., Buller R. M., Upton C. 2005; Complete coding sequences of the rabbitpox virus genome. J Gen Virol 86:2969–2977 [CrossRef]
    [Google Scholar]
  37. Li G., Chen N., Feng Z., Buller R. M., Osborne J., Harms T., Damon I., Upton C., Esteban D. J. 2006; Genomic sequence and analysis of a vaccinia virus isolate from a patient with a smallpox vaccine-related complication. Virol J 3:88 [CrossRef]
    [Google Scholar]
  38. Lin Y. Z., Ke X. H., Tam J. P. 1990; Growth inhibition by vaccinia virus growth factor. J Biol Chem 265:18884–18890
    [Google Scholar]
  39. Mahalingam S., Damon I. K., Lidbury B. A. 2004; 25 years since the eradication of smallpox: why poxvirus research is still relevant. Trends Immunol 25:636–639 [CrossRef]
    [Google Scholar]
  40. Massung R. F., Liu L. I., Qi J., Knight J. C., Yuran T. E., Kerlavage A. R., Parsons J. M., Venter J. C., Esposito J. J. 1994; Analysis of the complete genome of smallpox variola major virus strain Bangladesh-1975. Virology 201:215–240 [CrossRef]
    [Google Scholar]
  41. McCoy S. L., Kurtz S. E., Macarthur C. J., Trune D. R., Hefeneider S. H. 2005; Identification of a peptide derived from vaccinia virus A52R protein that inhibits cytokine secretion in response to TLR-dependent signaling and reduces in vivo bacterial-induced inflammation. J Immunol 174:3006–3014 [CrossRef]
    [Google Scholar]
  42. McFadden G., Graham K., Ellison K., Barry M., Macen J., Schreiber M., Mossman K., Nash P., Lalani A., Everett H. 1995; Interruption of cytokine networks by poxviruses: lessons from myxoma virus. J Leukoc Biol 57:731–738
    [Google Scholar]
  43. Meyer H., Rziha H. J. 1993; Characterization of the gene encoding the A-type inclusion protein of camelpox virus and sequence comparison with other orthopoxviruses. J Gen Virol 74:1679–1684 [CrossRef]
    [Google Scholar]
  44. Mohamed M. R., Latner D. R., Condit R. C., Niles E. G. 2001; Interaction between the J3R subunit of vaccinia virus poly(A) polymerase and the H4L subunit of the viral RNA polymerase. Virology 280:143–152 [CrossRef]
    [Google Scholar]
  45. Morikawa S., Sakiyama T., Hasegawa H., Saijo M., Maeda A., Kurane I., Maeno G., Kimura J., Hirama C. other authors 2005; An attenuated LC16m8 smallpox vaccine: analysis of full-genome sequence and induction of immune protection. J Virol 79:11873–11891 [CrossRef]
    [Google Scholar]
  46. Nash P., Barrett J., Cao J. X., Hota-Mitchell S., Lalani A. S., Everett H., Xu X. M., Robichaud J., Hnatiuk S. other authors 1999; Immunomodulation by viruses: the myxoma virus story. Immunol Rev 168:103–120 [CrossRef]
    [Google Scholar]
  47. Niles E. G., Christen L. 1993; Identification of the vaccinia virus mRNA guanyltransferase active site lysine. J Biol Chem 268:24986–24989
    [Google Scholar]
  48. Patel D. D., Pickup D. J., Joklik W. K. 1986; Isolation of cowpox virus A-type inclusions and characterization of their major protein component. Virology 149:174–189 [CrossRef]
    [Google Scholar]
  49. Pires de Miranda M., Reading P. C., Tscharke D. C., Murphy B. J., Smith G. L. 2003; The vaccinia virus kelch-like protein C2L affects calcium-independent adhesion to the extracellular matrix and inflammation in a murine intradermal model. J Gen Virol 84:2459–2471 [CrossRef]
    [Google Scholar]
  50. Reading P. C., Smith G. L. 2003; Vaccinia virus interleukin-18-binding protein promotes virulence by reducing gamma interferon production and natural killer and T-cell activity. J Virol 77:9960–9968 [CrossRef]
    [Google Scholar]
  51. Reading P. C., Khanna A., Smith G. L. 2002; Vaccinia virus CrmE encodes a soluble and cell surface tumor necrosis factor receptor that contributes to virus virulence. Virology 292:285–298 [CrossRef]
    [Google Scholar]
  52. Sanger F., Nicklen S., Coulson A. R. 1977; DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A 74:5463–5467 [CrossRef]
    [Google Scholar]
  53. Saraiva M., Alcami A. 2001; CrmE, a novel soluble tumor necrosis factor receptor encoded by poxviruses. J Virol 75:226–233 [CrossRef]
    [Google Scholar]
  54. Shchelkunov S. N., Massung R. F., Esposito J. J. 1995; Comparison of the genome DNA sequences of Bangladesh-1975 and India-1967 variola viruses. Virus Res 36:107–118 [CrossRef]
    [Google Scholar]
  55. Shchelkunov S. N., Totmenin A. V., Loparev V. N., Safronov P. F., Gutorov V. V., Chizhikov V. E., Knight J. C., Parsons J. M., Massung R. F., Esposito J. J. 2000; Alastrim smallpox variola minor virus genome DNA sequences. Virology 266:361–386 [CrossRef]
    [Google Scholar]
  56. Shchelkunov S. N., Totmenin A. V., Safronov P. F., Mikheev M. V., Gutorov V. V., Ryazankina O. I., Petrov N. A., Babkin I. V., Uvarova E. A. & other authors 2002; Analysis of the monkeypox virus genome. Virology 297:172–194 [CrossRef]
    [Google Scholar]
  57. Smith V. P., Bryant N. A., Alcami A. 2000; Ectromelia, vaccinia and cowpox viruses encode secreted interleukin-18-binding proteins. J Gen Virol 81:1223–1230
    [Google Scholar]
  58. Sonnhammer E. L., Durbin R. 1995; A dot-matrix program with dynamic threshold control suited for genomic DNA and protein sequence analysis. Gene 167:GC1–GC10 [CrossRef]
    [Google Scholar]
  59. Stack J., Haga I. R., Schroder M., Bartlett N. W., Maloney G., Reading P. C., Fitzgerald K. A., Smith G. L., Bowie A. G. 2005; Vaccinia virus protein A46R targets multiple Toll-like-interleukin-1 receptor adaptors and contributes to virulence. J Exp Med 201:1007–1018 [CrossRef]
    [Google Scholar]
  60. Sugimoto M., Yasuda A., Miki K., Morita M., Suzuki K., Uchida N., Hashizume S. 1985; Gene structures of low-neurovirulent vaccinia virus LC16m0, LC16m8, and their Lister original (LO) strains. Microbiol Immunol 29:421–428 [CrossRef]
    [Google Scholar]
  61. Symons J. A., Tscharke D. C., Price N., Smith G. L. 2002; A study of the vaccinia virus interferon-gamma receptor and its contribution to virus virulence. J Gen Virol 83:1953–1964
    [Google Scholar]
  62. Tone M., Thompson S. A., Tone Y., Fairchild P. J., Waldmann H. 1997; Regulation of IL-18 (IFN-gamma-inducing factor) gene expression. J Immunol 159:6156–6163
    [Google Scholar]
  63. Tscharke D. C., Reading P. C., Smith G. L. 2002; Dermal infection with vaccinia virus reveals roles for virus proteins not seen using other inoculation routes. J Gen Virol 83:1977–1986
    [Google Scholar]
  64. Tulman E. R., Afonso C. L., Lu Z., Zsak L., Kutish G. F., Rock D. L. 2004; The genome of canarypox virus. J Virol 78:353–366 [CrossRef]
    [Google Scholar]
  65. Tulman E. R., Delhon G., Afonso C. L., Lu Z., Zsak L., Sandybaev N. T., Kerembekova U. Z., Zaitsev V. L., Kutish G. F., Rock D. L. 2006; Genome of horsepox virus. J Virol 80:9244–9258 [CrossRef]
    [Google Scholar]
  66. Yeh W. W., Moss B., Wolffe E. J. 2000; The vaccinia virus A9L gene encodes a membrane protein required for an early step in virion morphogenesis. J Virol 74:9701–9711 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.82708-0
Loading
/content/journal/jgv/10.1099/vir.0.82708-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error