Characterization of Two Historic Smallpox Specimens from a Czech Museum
Language English Country Switzerland Media electronic
Document type Historical Article, Journal Article, Research Support, Non-U.S. Gov't
PubMed
28749451
PubMed Central
PMC5580457
DOI
10.3390/v9080200
PII: v9080200
Knihovny.cz E-resources
- Keywords
- evolution, historic specimen, next generation sequencing, phylogeny, smallpox, variola virus,
- MeSH
- History, 19th Century MeSH
- History, 20th Century MeSH
- DNA, Viral genetics MeSH
- Phylogeny MeSH
- Genome, Viral * MeSH
- Humans MeSH
- Evolution, Molecular MeSH
- Museums * MeSH
- Polymerase Chain Reaction MeSH
- Smallpox epidemiology history virology MeSH
- Proteomics MeSH
- Variola virus classification genetics MeSH
- High-Throughput Nucleotide Sequencing MeSH
- Check Tag
- History, 19th Century MeSH
- History, 20th Century MeSH
- Humans MeSH
- Publication type
- Journal Article MeSH
- Historical Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Geographicals
- Czech Republic MeSH
- Europe epidemiology MeSH
- India epidemiology MeSH
- Names of Substances
- DNA, Viral MeSH
Although smallpox has been known for centuries, the oldest available variola virus strains were isolated in the early 1940s. At that time, large regions of the world were already smallpox-free. Therefore, genetic information of these strains can represent only the very last fraction of a long evolutionary process. Based on the genomes of 48 strains, two clades are differentiated: Clade 1 includes variants of variola major, and clade 2 includes West African and variola minor (Alastrim) strains. Recently, the genome of an almost 400-year-old Lithuanian mummy was determined, which fell basal to all currently sequenced strains of variola virus on phylogenetic trees. Here, we determined two complete variola virus genomes from human tissues kept in a museum in Prague dating back 60 and 160 years, respectively. Moreover, mass spectrometry-based proteomic, chemical, and microscopic examinations were performed. The 60-year-old specimen was most likely an importation from India, a country with endemic smallpox at that time. The genome of the 160-year-old specimen is related to clade 2 West African and variola minor strains. This sequence likely represents a new endemic European variant of variola virus circulating in the midst of the 19th century in Europe.
Bundeswehr Institute of Microbiology Neuherbergstr 11 80937 Munich Germany
Genomics Core Facility EMBL Heidelberg Meyerhofstraße 1 69117 Heidelberg Germany
Institute of Molecular Genetics of the ASCR v v i Vídeňská 1083 142 20 Prague 4 Czech Republic
Military Health Institute Military Medical Agency Tychonova 1 160 01 Prague 6 Czech Republic
National Museum Department of Anthropology Václavské náměstí 68 115 79 Praha 1 Czech Republic
See more in PubMed
Fenner F., Henderson D.A., Arita I., Jezek Z., Ladnyi I.D. Smallpox. World Health Organ; Geneva, Switzerland: 1988.
Geddes A.M. The history of smallpox. Clin. Dermatol. 2006;24:152–157. doi: 10.1016/j.clindermatol.2005.11.009. PubMed DOI
Henderson D.A., Arita I. The Smallpox Threat: A Time to Reconsider Global Policy. Biosecur. Bioterror. Biodef. Strateg. Pract. Sci. 2014;12:117–121. doi: 10.1089/bsp.2014.1509.comm. PubMed DOI
Esposito J.J. Genome Sequence Diversity and Clues to the Evolution of Variola (Smallpox) Virus. Science. 2006;313:807–812. doi: 10.1126/science.1125134. PubMed DOI
Babkin V.I., Babkina N.I. A retrospective study of the orthopoxvirus molecular evolution. Infect. Genet. Evol. J. Mol. Epidemiol. Evol. Genet. Infect. Dis. 2012;12:1597–1604. doi: 10.1016/j.meegid.2012.07.011. PubMed DOI
Babkin I.V., Nepomnyashchikh T.S., Maksyutov R.A., Gutorov V.V., Babkina I.N., Shchelkunov S.N. Comparative analysis of variable regions in the variola virus genome. Mol. Biol. 2008;42:543–553. doi: 10.1134/S0026893308040092. PubMed DOI
Li Y., Carroll D.S., Gardner S.N., Walsh M.C., Vitalis E.A., Damon I.K. On the origin of smallpox: Correlating variola phylogenics with historical smallpox records. Proc. Natl. Acad. Sci. USA. 2007;104:15787–15792. doi: 10.1073/pnas.0609268104. PubMed DOI PMC
Babkin V.I., Shchelkunov N.S. [Molecular evolution of poxviruses] Genetika. 2008;44:1029–1044. doi: 10.1134/S1022795408080036. PubMed DOI
Shchelkunov S.N. How long ago did smallpox virus emerge? Arch. Virol. 2009;154:1865–1871. doi: 10.1007/s00705-009-0536-0. PubMed DOI
Duggan A.T., Perdomo M.F., Piombino-Mascali D., Marciniak S., Poinar D., Emery M.V., Buchmann J.P., Duchêne S., Jankauskas R., Humphreys M., et al. 17th Century Variola Virus Reveals the Recent History of Smallpox. Curr. Biol. 2016;26:3407–3412. doi: 10.1016/j.cub.2016.10.061. PubMed DOI PMC
Biagini P., Thèves C., Balaresque P., Géraut A., Cannet C., Keyser C., Nikolaeva D., Gérard P., Duchesne S., Orlando L., et al. Variola Virus in a 300-Year-Old Siberian Mummy. N. Engl. J. Med. 2012;367:2057–2059. doi: 10.1056/NEJMc1208124. PubMed DOI
Enserink M., Stone R. Dead Virus Walking. Science. 2002;295:2001–2005. doi: 10.1126/science.295.5562.2001. PubMed DOI
Fornaciari G., Marchetti A. Intact smallpox virus particles in an Italian mummy of sixteenth century. Lancet. 1986;328:625. doi: 10.1016/S0140-6736(86)92443-8. PubMed DOI
McCollum A.M., Li Y., Wilkins K., Karem K.L., Davidson W.B., Paddock C.D., Reynolds M.G., Damon I.K. Poxvirus Viability and Signatures in Historical Relics. Emerg. Infect. Dis. 2014;20:177–184. doi: 10.3201/eid2002.131098. PubMed DOI PMC
Schoepp R.J., Morin M.D., Martinez M.J., Kulesh D.A., Hensley L., Geisbert T.W., Brady D.R., Jahrling P.B. Detection and identification of Variola virus in fixed human tissue after prolonged archival storage. Lab. Investig. 2004;84:41–48. doi: 10.1038/labinvest.3700008. PubMed DOI
Thèves C., Biagini P., Crubézy E. The rediscovery of smallpox. Clin. Microbiol. Infect. 2014;20:210–218. doi: 10.1111/1469-0691.12536. PubMed DOI
Smrčka V., Kuželka V., Povýšil C. Atlas of Diseases in Dry Bones: Upper and Lower Extremities. Academia; Prague, Czech Republic: 2009. Introduction; pp. 15–33.
Fedele C.G., Negredo A., Molero F., Sanchez-Seco M.P., Tenorio A. Use of Internally Controlled Real-Time Genome Amplification for Detection of Variola Virus and Other Orthopoxviruses Infecting Humans. J. Clin. Microbiol. 2006;44:4464–4470. doi: 10.1128/JCM.00276-06. PubMed DOI PMC
Olson A.V., Laue T., Laker T.M., Babkin V.I., Drosten C., Shchelkunov N.S., Niedrig M., Damon K.I., Meyer H. Real-time PCR system for detection of orthopoxviruses and simultaneous identification of smallpox virus. J. Clin. Microbiol. 2004;42:1940–1946. doi: 10.1128/JCM.42.5.1940-1946.2004. PubMed DOI PMC
Damaso C.R.A., Esposito J.J., Condit R.C., Moussatché N. An Emergent Poxvirus from Humans and Cattle in Rio de Janeiro State: Cantagalo Virus May Derive from Brazilian Smallpox Vaccine. Virology. 2000;277:439–449. doi: 10.1006/viro.2000.0603. PubMed DOI
Pilin A., Čabala R., Pudil F., Bencko V. The Use of the d-, l- Aspartic Ratio in Decalcified Collagen from Human Dentin as an Estimator of Human Age. J. Forensic Sci. 2001;46:1228–1231. doi: 10.1520/JFS15126J. PubMed DOI
Li H. Aligning Sequence Reads, Clone Sequences and Assembly Contigs with BWA-MEM. Cornell University Library; Ithaca, NY, USA: 2013. ArXiv13033997 Q-Bio.
Bankevich A., Nurk S., Antipov D., Gurevich A.A., Dvorkin M., Kulikov S.A., Lesin M.V., Nikolenko I.S., Pham S., Prjibelski D.A., et al. SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. J. Comput. Mol. Cell Biol. 2012;19:455–477. doi: 10.1089/cmb.2012.0021. PubMed DOI PMC
Walker J.B., Abeel T., Shea T., Priest M., Abouelliel A., Sakthikumar S., Cuomo A.C., Zeng Q., Wortman J., Young K.S., Earl M.A. Pilon: An integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS ONE. 2014;9 doi: 10.1371/journal.pone.0112963. PubMed DOI PMC
Li H., Handsaker B., Wysoker A., Fennell T., Ruan J., Homer N., Marth G., Abecasis G., Durbin R. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25:2078–2079. doi: 10.1093/bioinformatics/btp352. PubMed DOI PMC
Katoh K., Standley D.M. MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability. Mol. Biol. Evol. 2013;30:772–780. doi: 10.1093/molbev/mst010. PubMed DOI PMC
Kumar S., Nei M., Dudley J., Tamura K. MEGA: A biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief. Bioinform. 2008;9:299–306. doi: 10.1093/bib/bbn017. PubMed DOI PMC
Tcherepanov V., Ehlers A., Upton C. Genome Annotation Transfer Utility (GATU): Rapid annotation of viral genomes using a closely related reference genome. BMC Genom. 2006;7:150. doi: 10.1186/1471-2164-7-150. PubMed DOI PMC
Upton C., Slack S., Hunter A.L., Ehlers A., Roper R.L. Poxvirus Orthologous Clusters: toward Defining the Minimum Essential Poxvirus Genome. J. Virol. 2003;77:7590–7600. doi: 10.1128/JVI.77.13.7590-7600.2003. PubMed DOI PMC
Drummond A.J., Suchard M.A., Xie D., Rambaut A. Bayesian Phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 2012;29:1969–1973. doi: 10.1093/molbev/mss075. PubMed DOI PMC
Drummond A.J., Ho S.Y.W., Phillips M.J., Rambaut A. Relaxed Phylogenetics and Dating with Confidence. PLoS Biol. 2006;4:e88. doi: 10.1371/journal.pbio.0040088. PubMed DOI PMC
Hasegawa M., Kishino H., Yano T. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J. Mol. Evol. 1985;22:160–174. doi: 10.1007/BF02101694. PubMed DOI
Wiśniewski J.R., Zougman A., Mann M. Combination of FASP and StageTip-based fractionation allows in-depth analysis of the hippocampal membrane proteome. J. Proteome Res. 2009;8:5674–5678. doi: 10.1021/pr900748n. PubMed DOI
MacLean B., Tomazela D.M., Shulman N., Chambers M., Finney G.L., Frewen B., Kern R., Tabb D.L., Liebler D.C., MacCoss M.J. Skyline: An open source document editor for creating and analyzing targeted proteomics experiments. Bioinform. Oxf. Engl. 2010;26:966–968. doi: 10.1093/bioinformatics/btq054. PubMed DOI PMC
Massung R.F., Knight J.C., Esposito J.J. Topography of Variola Smallpox Virus Inverted Terminal Repeats. Virology. 1995;211:350–355. doi: 10.1006/viro.1995.1416. PubMed DOI
Lefkowitz E.J., Wang C., Upton C. Poxviruses: Past, present and future. Virus Res. 2006;117:105–118. doi: 10.1016/j.virusres.2006.01.016. PubMed DOI
Smithson C., Purdy A., Verster A.J., Upton C. Prediction of Steps in the Evolution of Variola Virus Host Range. PLoS ONE. 2014;9:e91520. doi: 10.1371/journal.pone.0091520. PubMed DOI PMC
Turashvili G., Yang W., McKinney S., Kalloger S., Gale N., Ng Y., Chow K., Bell L., Lorette J., Carrier M., et al. Nucleic acid quantity and quality from paraffin blocks: defining optimal fixation, processing and DNA/RNA extraction techniques. Exp. Mol. Pathol. 2012;92:33–43. doi: 10.1016/j.yexmp.2011.09.013. PubMed DOI
Howat W.J., Wilson B.A. Tissue fixation and the effect of molecular fixatives on downstream staining procedures. Methods (San Diego Calif.) 2014;70:12–19. doi: 10.1016/j.ymeth.2014.01.022. PubMed DOI PMC
