Molecular characteristics of the capsid protein VP2 gene of canine parvovirus type 2 amplified from raccoon dogs in Hebei province, China

Abstract

Canine parvovirus type 2 (CPV-2) is currently circulating in domestic and wild animals, but our knowledge about CPV-2 infections in raccoon dogs is limited. In this study, VP2 gene sequences of CPV-2 were amplified from rectal swabs of 14 diarrhetic raccoon dogs (Nyctereutes procyonoides) in Hebei province, China, in 2016 and 2017. Phylogenetic analysis of the VP2 gene sequences revealed that most of these sequences (11 of 14) belonged to the same subclade as raccoon dog strain CPV-2/Raccoon_Dog/China/DP-1/16 isolated from Shandong province in 2016. A comparison of deduced amino acid sequences revealed presence of the substitutions S297A and S27T in 11 of those 14 sequences. I418T was observed in a minority of the sequences (4 of 14). In addition, A300D and T301I, P13S and I219V, and N419K were found in three of the sequences. This study shows that CPV-2 strains with different substitutions in their VP2 amino acid sequences were spreading among raccoon dogs in Hebei during 2016 and 2017 and suggests that further studies are needed to monitor the distribution of these strains in China.

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References

  1. 1.

    Allison AB, Harbison CE, Pagan I, Stucker KM, Kaelber JT, Brown JD, Ruder MG, Keel MK, Dubovi EJ, Holmes EC, Parrish CR (2012) Role of multiple hosts in the cross-species transmission and emergence of a pandemic parvovirus. J Virol 86:865–872

    CAS  Article  Google Scholar 

  2. 2.

    Allison AB, Kohler DJ, Fox KA, Brown JD, Gerhold RW, Shearn-Bochsler VI, Dubovi EJ, Parrish CR, Holmes EC (2013) Frequent cross-species transmission of parvoviruses among diverse carnivore hosts. J Virol 87:2342–2347

    CAS  Article  Google Scholar 

  3. 3.

    Allison AB, Kohler DJ, Ortega A, Hoover EA, Grove DM, Holmes EC, Parrish CR (2014) Host-specific parvovirus evolution in nature is recapitulated by in vitro adaptation to different carnivore species. PLoS Pathog 10:e1004475

    Article  Google Scholar 

  4. 4.

    Allison AB, Organtini LJ, Zhang S, Hafenstein SL, Holmes EC, Parrish CR (2016) Single mutations in the VP2 300 loop region of the three-fold spike of the carnivore parvovirus capsid can determine host range. J Virol 90:753–767

    CAS  Article  Google Scholar 

  5. 5.

    Appel MJ, Scott FW, Carmichael LE (1979) Isolation and immunisation studies of a canine parco-like virus from dogs with haemorrhagic enteritis. Vet Record 105:156–159

    CAS  Article  Google Scholar 

  6. 6.

    Buonavoglia C, Martella V, Pratelli A, Tempesta M, Cavalli A, Buonavoglia D, Bozzo G, Elia G, Decaro N, Carmichael L (2001) Evidence for evolution of canine parvovirus type 2 in Italy. J Gen Virol 82:3021

    CAS  Article  Google Scholar 

  7. 7.

    Callaway HM, Welsch K, Weichert W, Allison AB, Hafenstein SL, Huang K, Iketani S, Parrish CR (2018) Complex and dynamic interactions between parvovirus capsids, transferrin receptors and antibodies control cell infection and host range. J Virol 92:e00460–e1418

    CAS  Article  Google Scholar 

  8. 8.

    Chapman MS, Rossmann MG (1993) Structure, sequence, and function correlations among parvoviruses. Virology 194:491–508

    CAS  Article  Google Scholar 

  9. 9.

    Cotmore SF, Agbandje-McKenna M, Canuti M, Chiorini JA, Eis-Hubinger AM, Hughes J, Mietzsch M, Modha S, Ogliastro M, Penzes JJ, Pintel DJ, Qiu J, Soderlund-Venermo M, Tattersall P, Tijssen P, Ictv Report C (2019) ICTV virus taxonomy profile: parvoviridae. J Gen Virol 100:367–368

    CAS  Article  Google Scholar 

  10. 10.

    De la Torre D, Mafla E, Puga B, Erazo L, Astolfi-Ferreira C, Ferreira AP (2018) Molecular characterization of canine parvovirus variants (CPV-2a, CPV-2b, and CPV-2c) based on the VP2 gene in affected domestic dogs in Ecuador. Veterinary World 11:480–487

    Article  Google Scholar 

  11. 11.

    Decaro N, Desario C, Miccolupo A, Campolo M, Parisi A, Martella V, Amorisco F, Lucente MS, Lavazza A, Buonavoglia C (2008) Genetic analysis of feline panleukopenia viruses from cats with gastroenteritis. J Gen Virol 89:2290–2298

    CAS  Article  Google Scholar 

  12. 12.

    Deng X, Zhang J, Su J, Liu H, Cong Y, Zhang L, Zhang K, Shi N, Lu R, Yan X (2018) A multiplex PCR method for the simultaneous detection of three viruses associated with canine viral enteric infections. Arch Virol 163:2133–2138

    CAS  Article  Google Scholar 

  13. 13.

    Hoelzer K, Shackelton LA, Parrish CR, Holmes EC (2008) Phylogenetic analysis reveals the emergence, evolution and dispersal of carnivore parvoviruses. J Gen Virol 89:2280–2289

    CAS  Article  Google Scholar 

  14. 14.

    Jeoung SY, Ahn SJ, Kim D (2008) Genetic analysis of VP2 gene of canine parvovirus isolates in Korea. J Vet Med Sci 70:719

    CAS  Article  Google Scholar 

  15. 15.

    Kaelber JT, Demogines A, Harbison CE, Allison AB, Goodman LB, Ortega AN, Sawyer SL, Parrish CR (2012) Evolutionary reconstructions of the transferrin receptor of caniforms supports canine parvovirus being a re-emerged and not a novel pathogen in dogs. PLoS Pathog 8:e1002666

    CAS  Article  Google Scholar 

  16. 16.

    Kang BK, Song DS, Lee CS, Jung KI, Park SJ, Kim EM, Park BK (2008) Prevalence and genetic characterization of canine parvoviruses in Korea. Virus Genes 36:127–133

    CAS  Article  Google Scholar 

  17. 17.

    Kumar S, Stecher G, Li M, Knyaz C, Tamura K, Battistuzzi FU (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549

    CAS  Article  Google Scholar 

  18. 18.

    Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    CAS  Article  Google Scholar 

  19. 19.

    Lee DW, Allison AB, Bacon KB, Parrish CR, Daniel S (2016) Single-particle tracking shows that a point mutation in the carnivore parvovirus capsid switches binding between host-specific transferrin receptors. J Virol 90:4849–4853

    Article  Google Scholar 

  20. 20.

    Mira F, Purpari G, Di Bella S, Colaianni ML, Schiro G, Chiaramonte G, Gucciardi F, Pisano P, Lastra A, Decaro N, Guercio A (2019) Spreading of canine parvovirus type 2c mutants of Asian origin in southern Italy. Transbound Emerg Dis 66:2297–2304

    CAS  Article  Google Scholar 

  21. 21.

    Nelson CD, Minkkinen E, Bergkvist M, Hoelzer K, Fisher M, Bothner B, Parrish CR (2008) Detecting small changes and additional peptides in the canine parvovirus capsid structure. J Virol 82:10397–10407

    CAS  Article  Google Scholar 

  22. 22.

    Parrish CR, O'Connell PH, Evermann JF, Carmichael LE (1985) Natural variation of canine parvovirus. Science 230:1046–1048

    CAS  Article  Google Scholar 

  23. 23.

    Parrish CR, Have P, Foreyt WJ, Evermann JF, Senda M, Carmichael LE (1988) The global spread and replacement of canine parvovirus strains. J Gen Virol 69(Pt 5):1111

    Article  Google Scholar 

  24. 24.

    Pereira CA, Leal ES, Durigon EL (2007) Selective regimen shift and demographic growth increase associated with the emergence of high-fitness variants of canine parvovirus. Infect Genet Evol 7:399–409

    CAS  Article  Google Scholar 

  25. 25.

    Shackelton LA, Parrish CR, Uwe T, Holmes EC (2005) High rate of viral evolution associated with the emergence of carnivore parvovirus. Proc Natl Acad Sci USA 102:379–384

    CAS  Article  Google Scholar 

  26. 26.

    Son K, Lee SM, Kim YS, Kim YK, Lee SY, Jheong WH, Oem JK (2018) Genetic characterization of canine parvovirus 2 detected in wild raccoon dogs (Nyctereutes procyonoides) in the Republic of Korea. J Wildl Dis 5:512–515

    Google Scholar 

  27. 27.

    Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of Mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526

    CAS  Google Scholar 

  28. 28.

    Truyen U (1999) Emergence and recent evolution of canine parvovirus. Vet Microbiol 69:47–50

    CAS  Article  Google Scholar 

  29. 29.

    Voorhees IEH, Lee H, Allison AB, Lopez-Astacio R, Goodman LB, Oyesola OO, Omobowale O, Fagbohun O, Dubovi EJ, Hafenstein SL, Holmes EC, Parrish CR (2019) Limited intrahost diversity and background evolution accompany 40 years of canine parvovirus host adaptation and spread. J Virol 94:e01162–e11119

    Article  Google Scholar 

  30. 30.

    Yu J, Qian Z, Diao F, Teng C, Peng H, Shang Y, Zhao Y, Wang J, Jiang S, Xie Z (2018) Emergence of novel canine parvovirus type 2 and its pathogenesis in raccoon dogs. Vet Microbiol 216:7–12

    CAS  Article  Google Scholar 

  31. 31.

    Yuan W, Parrish CR (2000) Comparison of two single-chain antibodies that neutralize canine parvovirus: analysis of an antibody-combining site and mechanisms of neutralization. Virology 269:471–480

    CAS  Article  Google Scholar 

  32. 32.

    Zhao H, Wang J, Jiang Y, Cheng Y, Lin P, Zhu H, Han G, Yi L, Zhang S, Guo L, Cheng S (2017) Typing of canine parvovirus strains circulating in north-east China. Transbound Emerg Dis 64:495–503

    CAS  Article  Google Scholar 

  33. 33.

    Zhou P, Zeng W, Zhang X, Li S (2017) The genetic evolution of canine parvovirus—a new perspective. PLoS ONE 12:e0175035

    Article  Google Scholar 

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Acknowledgements

This work was supported by the National Key R&D Program of China (2017YFD0501600), the National Natural Science Foundation of China (NSFC) [31702275 to H.Z.], the Central Committee Guides Local Science and Technology Development Project (18246629G) and the Central Public-Interest Scientific Institution Basal Research Fund of Chinese Academy of Agricultural Sciences (1610342018017).

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Correspondence to Weiquan Liu or Xijun Yan.

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Lu, R., Yu, Y., Zhu, X. et al. Molecular characteristics of the capsid protein VP2 gene of canine parvovirus type 2 amplified from raccoon dogs in Hebei province, China. Arch Virol 165, 2453–2459 (2020). https://doi.org/10.1007/s00705-020-04714-3

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