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Comparison and phylogenetic analysis of cowpox viruses isolated from cats and humans in Fennoscandia

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Abstract

Cowpox virus (CPXV), a member of the genus Orthopoxvirus (OPV), has reservoirs in small mammals and may cause disease in humans, felidae and other animals. In this study we compared CPXVs isolated from humans and cats in Fennoscandia by restriction enzyme and DNA sequence analysis. The HindIII restriction profiles clearly distinguished geographically distinct CPXV isolates, whereas only minor differences were found between the profiles of geographically linked isolates. The complete gene sequences encoding the cytokine response modifier B, the hemagglutinin and the Chinese hamster ovary host range protein were determined for the same isolates and included in phylogenetic analysis. By including representative OPV sequences from GenBank, detailed comparative analyses were performed showing pronounced heterogeneity among CPXVs compared to members of other OPV species. However, a close relationship between the Norwegian (3 of 4 isolates) and Swedish isolates was detected, whereas the isolate from Finland was more closely related to a Russian isolate for all three genes compared. We infer that the investigated CPXVs have distinct evolutionary histories in different rodent lineages.

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References

  1. Antoine G, Scheiflinger F, Dorner F, Falkner FG (1998) The complete genomic sequence of the modified vaccinia Ankara strain: comparison with other orthopoxviruses. Virology 244:365–396

    Article  PubMed  CAS  Google Scholar 

  2. Babkin IV, Petrov NA, Kablova GV, Petrov VS, Shchelkunov SN, Sandakhchiev LS (1997) The study of the variability of A27L and A56R orthopoxvirus genes. Dokl Akad Nauk 357:117–122

    PubMed  CAS  Google Scholar 

  3. Baroudy BM, Moss B (1982) Sequence homologies of diverse length tandem repetitions near ends of vaccinia virus genome suggest unequal crossing over. Nucleic Acids Res 10:5673–5679

    Article  PubMed  CAS  Google Scholar 

  4. Baxby D, Bennett M (1994) Cowpox virus. In: Webster RG, Granhoff A (eds) Encyclopedia of virology. Academic Press, London, pp 261–267

    Google Scholar 

  5. Baxby D, Bennett M, Getty B (1994) Human cowpox 1969–93: a review based on 54 cases. Br J Dermatol 131:598–607

    Article  PubMed  CAS  Google Scholar 

  6. Boulanger D, Crouch A, Brochier B, Bennett M, Clement J, Gaskell RM, Baxby D, Pastoret PP (1996) Serological survey for orthopoxvirus infection of wild mammals in areas where a recombinant rabies virus is used to vaccinate foxes. Vet Rec 138:247–249

    PubMed  CAS  Google Scholar 

  7. Chantrey J, Meyer H, Baxby D, Begon M, Bown KJ, Hazel SM, Jones T, Montgomery WI, Bennett M (1999) Cowpox: reservoir hosts and geographic range. Epidemiol Infect 122:455–460

    Article  PubMed  CAS  Google Scholar 

  8. Cronqvist J, Ekdahl K, Kjartansdottir A, Bauer B, Klinker M (1991) Cowpox—a cat disease in man. Lakartidningen 88:2605–2606

    PubMed  CAS  Google Scholar 

  9. Crouch AC, Baxby D, McCracken CM, Gaskell RM, Bennett M (1995) Serological evidence for the reservoir hosts of cowpox virus in British wildlife. Epidemiol Infect 115:185–191

    Article  PubMed  CAS  Google Scholar 

  10. Czerny CP, Zeller Lue C, Eis Hubinger AM, Kaaden OR, Meyer H (1997) Characterization of a cowpox-like orthopox virus which had caused a lethal infection in man. Arch Virol Suppl 13:13–24

    PubMed  CAS  Google Scholar 

  11. Damaso CR, Esposito JJ, Condit RC, Moussatché N (2000) An emergent poxvirus from humans and cattle in Rio de Janeiro State: Cantagalo virus may derive from Brazilian smallpox vaccine. Virology 277:439–449

    Google Scholar 

  12. Drillien R, Spehner D, Kirn A (1978) Host range restriction of vaccinia virus in Chinese hamster ovary cells: relationship to shutoff of protein synthesis. J Virol 28:843–850

    PubMed  CAS  Google Scholar 

  13. Dumbell K, Richardson M (1993) Virological investigations of specimens from buffaloes affected by buffalopox in Maharashtra State, India between 1985 and 1987. Arch Virol 128:257–267

    Article  PubMed  CAS  Google Scholar 

  14. Esposito J, Condit R, Obijeski J (1981) The preparation of orthopoxvirus DNA. J Virol Methods 2:175–179

    Article  PubMed  CAS  Google Scholar 

  15. Esposito J, Fenner F (2001) Poxviruses. In: Roizman B, Howley P, Straus S, Martin M, DE G, Lamb R, Knipe D (eds) Fields virology. Lippincott Williams & Wilkins, Philadelphia

    Google Scholar 

  16. Fenner F, Henderson DA, Arita I, Jezek Z, Ladnyj ID (1988) Smallpox and its eradication. World Health Organization, Geneva

    Google Scholar 

  17. Gubser C, Smith GL (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

    PubMed  CAS  Google Scholar 

  18. Gubser C, Hue S, Kellam P, Smith GL (2004) Poxvirus genomes: a phylogenetic analysis. J Gen Virol 85:105–117

    Article  PubMed  CAS  Google Scholar 

  19. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  20. Hansen H, Sandvik T, Tryland M, Olsvik O, Traavik T (1999) Comparison of thymidine kinase and A-type inclusion protein gene sequences from Norwegian and Swedish cowpox virus isolates. Apmis 107:667–675

    PubMed  CAS  Google Scholar 

  21. Heymann DL, Szczeniowski M, Esteves K (1998) Re-emergence of monkeypox in Africa: a review of the past six years. Br Med Bull 54:693–702

    PubMed  CAS  Google Scholar 

  22. Horling J, Lundkvist A, Jaarola M, Plyusnin A, Tegelstrom H, Persson K, Lehvaslaiho H, Hornfeldt B, Vaheri A, Niklasson B (1996) Distribution and genetic heterogeneity of Puumala virus in Sweden. J Gen Virol 77:2555–2562

    Article  PubMed  Google Scholar 

  23. Hu FQ, Smith CA, Pickup DJ (1994) Cowpox virus contains two copies of an early gene encoding a soluble secreted form of the type II TNF receptor. Virology 204:343–356

    Article  PubMed  CAS  Google Scholar 

  24. Hutin YJ, Williams RJ, Malfait P, Pebody R, Loparev VN, Ropp SL, Rodriguez M, Knight JC, Tshioko FK, Khan AS, Szczeniowski MV, Esposito JJ (2001) Outbreak of human monkeypox, Democratic Republic of Congo, 1996 to 1997. Emerg Infect Dis 7:434–438

    PubMed  CAS  Google Scholar 

  25. Jezek Z, Grab B, Paluku KM, Szczeniowski MV (1988) Human monkeypox: disease pattern, incidence and attack rates in a rural area of northern Zaire. Trop Geogr Med 40:73–83

    PubMed  CAS  Google Scholar 

  26. Jaarola M, Tegelstrom H, Fredga K (1999) Colonization history in Fennoscandian rodents. Biol J Linnean Soc 68:113–127

    Article  Google Scholar 

  27. Kaplan C, Healing TD, Evans N, Healing L, Prior A (1980) Evidence of infection by viruses in small British field rodents. J Hyg Lond 84:285–294

    Article  PubMed  CAS  Google Scholar 

  28. Kolhapure RM, Deolankar RP, Tupe CD, Raut CG, Basu A, Dama BM, Pawar SD, Joshi MV, Padbidri VS, Goverdhan MK, Banerjee K (1997) Investigation of buffalopox outbreaks in Maharashtra State during 1992–1996. Indian J Med Res 106:441–446

    PubMed  CAS  Google Scholar 

  29. Loparev VN, Massung RF, Esposito JJ, Meyer H (2001) Detection and differentiation of old world orthopoxviruses: restriction fragment length polymorphism of the crmB gene region. J Clin Microbiol 39:94–100

    Article  PubMed  CAS  Google Scholar 

  30. Lundkvist A, Wiger D, Horling J, Sjolander KB, Plyusnina A, Mehl R, Vaheri A, Plyusnin A (1998) Isolation and characterization of Puumala hantavirus from Norway: evidence for a distinct phylogenetic sublineage. J Gen Virol 79:2603–2614

    PubMed  CAS  Google Scholar 

  31. Meyer H, Schay C, Mahnel H, Pfeffer M (1999) Characterization of orthopoxviruses isolated from man and animals in Germany. Arch Virol 144:491–501

    Article  PubMed  CAS  Google Scholar 

  32. Naidoo J, Baxby D, Bennett M, Gaskell RM, Gaskell CJ (1992) Characterization of orthopoxviruses isolated from feline infections in Britain. Arch Virol 125:261–272

    Article  PubMed  CAS  Google Scholar 

  33. Oie M, Shida H, Ichihashi Y (1990) The function of the vaccinia hemagglutinin in the proteolytic activation of infectivity. Virology 176:494–504

    Article  PubMed  CAS  Google Scholar 

  34. Ortiz MA, Paez E (1994) Identification of viral membrane proteins required for cell fusion and viral dissemination that are modified during vaccinia virus persistence. Virology 198:155–168

    Article  PubMed  CAS  Google Scholar 

  35. Pelkonen PM, Tarvainen K, Hynninen A, Kallio ER, Henttonen K, Palva A, Vaheri A, Vapalahti O (2003) Cowpox with severe generalized eruption, Finland. Emerg Infect Dis 9:1458–1461

    PubMed  Google Scholar 

  36. Perkus ME, Goebel SJ, Davis SW, Johnson GP, Limbach K, Norton EK, Paoletti E (1990) Vaccinia virus host range genes. Virology 179:276–286

    Article  PubMed  CAS  Google Scholar 

  37. Pulford DJ, Meyer H, Ulaeto D (2002) Orthologs of the vaccinia A13L and A36R virion membrane protein genes display diversity in species of the genus Orthopoxvirus. Arch Virol 147:995–1015

    Article  PubMed  CAS  Google Scholar 

  38. Ropp SL, Jin Q, Knight JC, Massung RF, Esposito JJ (1995) PCR strategy for identification and differentiation of small pox and other orthopoxviruses. J Clin Microbiol 33:2069–2076

    PubMed  CAS  Google Scholar 

  39. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  40. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbour Laboratory, NY

    Google Scholar 

  41. Sandvik T, Tryland M, Hansen H, Mehl R, Moens U, Olsvik O, Traavik T (1998) Naturally occurring orthopoxviruses: potential for recombination with vaccine vectors. J Clin Microbiol 36:2542–2547

    PubMed  CAS  Google Scholar 

  42. Shchelkunov S, Totmenin A, Kolosova I (2002) Species-specific differences in organization of orthopoxvirus kelch- like proteins. Virus Genes 24:157–162

    Article  PubMed  CAS  Google Scholar 

  43. Shchelkunov SN, Safronov PF, Totmenin AV, Petrov NA, Ryazankina OI, Gutorov VV, Kotwal GJ (1998) The genomic sequence analysis of the left and right species-specific terminal region of a cowpox virus strain reveals unique sequences and a cluster of intact ORFs for immunomodulatory and host range proteins. Virology 243:432–460

    Article  PubMed  CAS  Google Scholar 

  44. Shchelkunov SN, Totmenin AV, Loparev VN, Safronov PF, Gutorov VV, Chizhikov VE, Knight JC, Parsons JM, Massung RF, Esposito JJ (2000) Alastrim smallpox variola minor virus genome DNA sequences. Virology 266:361–386

    Article  PubMed  CAS  Google Scholar 

  45. Shchelkunov SN, Totmenin AV, Babkin IV, Safronov PF, Ryazankina OI, Petrov NA, Gutorov VV, Uvarova EA, Mikheev MV, Sisler JR, Esposito JJ, Jahrling PB, Moss B, Sandakhchiev LS (2001) Human monkeypox and smallpox viruses: genomic comparison. FEBS Lett 509:66–70

    Article  PubMed  CAS  Google Scholar 

  46. Shchelkunov SN, Totmenin AV, Safronov PF, Mikheev MV, Gutorov VV, Ryazankina OI, Petrov NA, Babkin IV, Uvarova EA, Sandakhchiev LS, Sisler JR, Esposito JJ, Damon IK, Jahrling PB, Moss B (2002) Analysis of the monkeypox virus genome. Virology 297:172–194

    Article  PubMed  CAS  Google Scholar 

  47. Shida H (1986) Nucleotide sequence of the vaccinia virus hemagglutinin gene. Virology 150:451–462

    Article  PubMed  CAS  Google Scholar 

  48. Spehner D, Gillard S, Drillien R, Kirn A (1988) A cowpox virus gene required for multiplication in Chinese hamster ovary cells. J Virol 62:1297–1304

    PubMed  CAS  Google Scholar 

  49. Sutter G, Wyatt LS, Foley PL, Bennink JR, Moss B (1994) A recombinant vector derived from the host range-restricted and highly attenuated MVA strain of vaccinia virus stimulates protective immunity in mice to influenza virus. Vaccine 12:1032–1040

    Article  PubMed  CAS  Google Scholar 

  50. Tryland M, Myrmel H, Holtet L, Haukenes G, Traavik T (1998) Clinical cowpox cases in Norway. Scand J Infect Dis 30:301–303

    Article  PubMed  CAS  Google Scholar 

  51. Tryland M, Sandvik T, Hansen H, Haukenes G, Holtet L, Bennett M, Mehl R, Moens U, Olsvik O, Traavik T (1998) Characteristics of four cowpox virus isolates from Norway and Sweden. Apmis 106:623–635

    Article  PubMed  CAS  Google Scholar 

  52. Tryland M, Sandvik T, Mehl R, Bennett M, Traavik T, Olsvik O (1998) Serosurvey for orthopoxviruses in rodents and shrews from Norway. J Wildl Dis 34:240–250

    PubMed  CAS  Google Scholar 

  53. Wittek R, Muller HK, Wyler R (1978) Length heterogeneity in the DNA of vaccinia virus is eliminated on cloning the virus. FEBS Lett 90:41–46

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Lisbeth Holtet (Bergen Veterinary Clinic, Norway), Gabriel Ånestad (National Institute of Public Health, Norway), Morten Tryland (Norwegian School of Veterinary Science, Norway), Olli Vapalahti (Haartman Institute, Finland) and Bernard Moss (National Institute of Allergy and Infectious Diseases, USA) for virus isolates. We also thank Berit Tømmerås and Randi Olsen (University of Tromsø, Norway) for technical assistance. This work was supported by the Norwegian Research Council and by the University of Tromsø, Norway.

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Authors and Affiliations

  1. Department of Molecular Biotechnology, Institute of Medical Biology, University of Tromsø, 9037, Tromsø, Norway

    Hilde Hansen

  2. Department of Microbiology and Virology, Institute of Medical Biology, University of Tromsø, 9037, Tromsø, Norway

    Hilde Hansen & Malachy Ifeanyi Okeke

  3. Department of Medical Genetics, Institute of Clinical Medicine, University of Tromsø, 9037, Tromsø, Norway

    Øivind Nilssen

  4. Department of Medical Genetics, University Hospital of North Norway, 9038, Tromsø, Norway

    Øivind Nilssen

  5. Institute of Pharmacy, University of Tromsø, 9037, Tromsø, Norway

    Terje Traavik

  6. GenØk-Centre for Biosafety, The Science Park, 9294, Tromsø, Norway

    Malachy Ifeanyi Okeke & Terje Traavik

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  1. Hilde Hansen
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  2. Malachy Ifeanyi Okeke
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  3. Øivind Nilssen
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  4. Terje Traavik
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Correspondence to Hilde Hansen or Terje Traavik.

Additional information

Nucleotide sequence data reported are available in the GenBank databases under the accession number FJ769336–FJ769355.

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Hansen, H., Okeke, M.I., Nilssen, Ø. et al. Comparison and phylogenetic analysis of cowpox viruses isolated from cats and humans in Fennoscandia. Arch Virol 154, 1293–1302 (2009). https://doi.org/10.1007/s00705-009-0442-5

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