Genomic sequence of a clonal isolate of the vaccinia virus Lister strain employed for smallpox vaccination in France and its comparison to other orthopoxviruses
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.
AlcamiA.,
SymonsJ. A.,
SmithG. 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]
AlejoA.,
Ruiz-ArguelloM. B.,
HoY.,
SmithV. P.,
SaraivaM.,
AlcamiA.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]
AmegadzieB. Y.,
AhnB. Y.,
MossB.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
AntoineG.,
ScheiflingerF.,
DornerF.,
FalknerF. G.1998; The complete genomic sequence of the modified vaccinia Ankara strain: comparison with other orthopoxviruses. Virology 244:365–396[CrossRef]
ChenN.,
DanilaM. I.,
FengZ.,
BullerR. M.,
WangC.,
HanX.,
LefkowitzE. J.,
UptonC.2003; The genomic sequence of ectromelia virus, the causative agent of mousepox. Virology 317:165–186[CrossRef]
de CarlosA.,
PaezE.1991; Isolation and characterization of mutants of vaccinia virus with a modified 94-kDa inclusion protein. Virology 185:768–778[CrossRef]
DiPernaG.,
StackJ.,
BowieA. G.,
BoydA.,
KotwalG.,
ZhangZ.,
ArvikarS.,
LatzE.,
FitzgeraldK. A.,
MarshallW. 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]
GaltierN.,
GouyM.,
GautierC.1996; SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci 12:543–548
GeshelinP.,
BernsK. I.1974; Characterization and localization of the naturally occurring cross-links in vaccinia virus DNA. J Mol Biol 88:785–796[CrossRef]
GoebelS. J.,
JohnsonG. P.,
PerkusM. E.,
DavisS. W.,
WinslowJ. P.,
PaolettiE.1990; The complete DNA sequence of vaccinia virus. Virology 179:247–266. 517–563
GubserC.,
SmithG. 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
GubserC.,
BergamaschiD.,
HollinsheadM.,
LuX.,
van KuppeveldF. J.,
SmithG. L.2007; A new inhibitor of apoptosis from vaccinia virus and eukaryotes. PloS Pathog 3:e17[CrossRef]
Herrero-MartinezE.,
RobertsK. L.,
HollinsheadM.,
SmithG. 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]
KahmannJ. D.,
WeckingD. A.,
PutterV.,
LowenhauptK.,
KimY. G.,
SchmiederP.,
OschkinatH.,
RichA.,
SchadeM.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]
KettleS.,
BlakeN. W.,
LawK. M.,
SmithG. 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]
KretzschmarM.,
WallingaJ.,
TeunisP.,
XingS.,
MikolajczykR.2006; Frequency of adverse events after vaccination with different vaccinia strains. PLoS Med 3:e272[CrossRef]
LanglandJ. O.,
JacobsB. L.2002; The role of the PKR-inhibitory genes, E3L and K3L, in determining vaccinia virus host range. Virology 299:133–141[CrossRef]
LeeL. G.,
SpurgeonS. L.,
HeinerC. R.,
BensonS. C.,
RosenblumB. B.,
MenchenS. M.,
GrahamR. J.,
ConstantinescuA.,
UpadhyaK. G.,
CasselJ. M.1997; New energy transfer dyes for DNA sequencing. Nucleic Acids Res 25:2816–2822[CrossRef]
LiG.,
ChenN.,
FengZ.,
BullerR. M.,
OsborneJ.,
HarmsT.,
DamonI.,
UptonC.,
EstebanD. 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]
MahalingamS.,
DamonI. K.,
LidburyB. A.2004; 25 years since the eradication of smallpox: why poxvirus research is still relevant. Trends Immunol 25:636–639[CrossRef]
MassungR. F.,
LiuL. I.,
QiJ.,
KnightJ. C.,
YuranT. E.,
KerlavageA. R.,
ParsonsJ. M.,
VenterJ. C.,
EspositoJ. J.1994; Analysis of the complete genome of smallpox variola major virus strain Bangladesh-1975. Virology 201:215–240[CrossRef]
McCoyS. L.,
KurtzS. E.,
MacarthurC. J.,
TruneD. R.,
HefeneiderS. 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]
MeyerH.,
RzihaH. 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]
MohamedM. R.,
LatnerD. R.,
ConditR. C.,
NilesE. 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]
PatelD. D.,
PickupD. J.,
JoklikW. K.1986; Isolation of cowpox virus A-type inclusions and characterization of their major protein component. Virology 149:174–189[CrossRef]
Pires de MirandaM.,
ReadingP. C.,
TscharkeD. C.,
MurphyB. J.,
SmithG. 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]
ReadingP. C.,
SmithG. 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]
ShchelkunovS. N.,
MassungR. F.,
EspositoJ. J.1995; Comparison of the genome DNA sequences of Bangladesh-1975 and India-1967 variola viruses. Virus Res 36:107–118[CrossRef]
SonnhammerE. L.,
DurbinR.1995; A dot-matrix program with dynamic threshold control suited for genomic DNA and protein sequence analysis. Gene 167:GC1–GC10[CrossRef]
StackJ.,
HagaI. R.,
SchroderM.,
BartlettN. W.,
MaloneyG.,
ReadingP. C.,
FitzgeraldK. A.,
SmithG. L.,
BowieA. 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]
SymonsJ. A.,
TscharkeD. C.,
PriceN.,
SmithG. L.2002; A study of the vaccinia virus interferon-gamma receptor and its contribution to virus virulence. J Gen Virol 83:1953–1964
TscharkeD. C.,
ReadingP. C.,
SmithG. L.2002; Dermal infection with vaccinia virus reveals roles for virus proteins not seen using other inoculation routes. J Gen Virol 83:1977–1986
YehW. W.,
MossB.,
WolffeE. 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]
Genomic sequence of a clonal isolate of the vaccinia virus Lister strain employed for smallpox vaccination in France and its comparison to other orthopoxviruses