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Archives of Virology

, Volume 163, Issue 5, pp 1241–1251 | Cite as

Genetic diversity and phylogenetic analysis of Aleutian mink disease virus isolates in north-east China

  • Xue Leng
  • Dongxu Liu
  • Jianming Li
  • Kun Shi
  • Fanli Zeng
  • Ying Zong
  • Yi Liu
  • Zhibo Sun
  • Shanshan Zhang
  • Yadong Liu
  • Rui Du
Original Article
  • 85 Downloads

Abstract

Aleutian mink disease is the most important disease in the mink-farming industry worldwide. So far, few large-scale molecular epidemiological studies of AMDV, based on the NS1 and VP2 genes, have been conducted in China. Here, eight new Chinese isolates of AMDV from three provinces in north-east China were analyzed to clarify the molecular epidemiology of AMDV. The seroprevalence of AMDV in north-east China was 41.8% according to counterimmuno-electrophoresis. Genetic variation analysis of the eight isolates showed significant non-synonymous substitutions in the NS1 and VP2 genes, especially in the NS1 gene. All eight isolates included the caspase-recognition sequence NS1:285 (DQTD↓S), but not the caspase recognition sequence NS1:227 (INTD↓S). The LN1 and LN2 strains had a new 10-amino-acid deletion in-between amino acids 28–37, while the JL3 strain had a one-amino-acid deletion at position 28 in the VP2 protein, compared with the AMDV-G strain. Phylogenetic analysis based on most of NS1 (1755 bp) and complete VP2 showed that the AMDV genotypes did not cluster according to their pathogenicity or geographic origin. Local and imported ADMV species are all prevalent in mink-farming populations in the north-east of China. This is the first study to report the molecular epidemiology of AMDV in north-east China based on most of NS1 and the complete VP2, and further provides information about polyG deletions and new variations in the amino acid sequences of NS1 and VP2 proteins. This report is a good foundation for further study of AMDV in China.

Notes

Acknowledgements

This work was supported by a grant from the National Natural Science Foundation of China (31272565).

Compliance with ethical standards

Conflict of interest

All authors declare that they have no conflict of interest.

Ethical approval

All animal studies were approved by the ethics committee of the Jilin Institute of Endemic Disease Control and Prevention. All the mink were treated in strict accordance with the Guidelines for the Use and Care of Laboratory Animals from the Chinese CDC and the Rules for the Implementation of Laboratory Animal Medicine (1998) from the Ministry of Health, China.

Informed consent

Informed consent was obtained from individual farmers for the samples used in this study.

References

  1. 1.
    Best SM, Shelton JF, Pompey JM, Wolfinbarger JB, Bloom MB (2003) Caspase cleavage of the nonstructural protein NS1 mediates replication of Aleutian mink disease Parvovirus. J Virol 77:5305–5312CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Best SM, Wolfinbarger JB, Bloom ME (2002) Caspase activation is required for permissive replication of Aleutian mink disease parvovirus in vitro. Virology 292:224–234CrossRefPubMedGoogle Scholar
  3. 3.
    Bloom ME, Alexandersen S, Garon CF, Mori S, Wei W, Perryman S, Wolfinbarger JB (1990) Nucleotide sequence of the 50-terminal palindrome of Aleutian mink disease parvovirus and construction of an infectious molecular clone. J Virol 64:3551–3556PubMedPubMedCentralGoogle Scholar
  4. 4.
    Bloom ME, Best SM, Yayes SF, Wells RD, Wolfinbarger JB, Mckenna R, Agbandje-mckenna M (2001) Identification of Aleutian mink disease parvovirus capsid sequences mediating antibody-dependent enhancement of infection, virus neutralization, and immune complex formation. J Virol 75:11116–11127CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Bloom ME, Fox JM, Berry BD, Oie KL, Wolfinbarger JB (1998) Construction of pathogenic molecular clones of Aleutian mink disease parvovirus (ADV) that replicate both in vivo and in vitro. Virology 251:288–296CrossRefPubMedGoogle Scholar
  6. 6.
    Bloom ME, Kanno H, Mori S, Wolfinbarger JB (1994) Aleutian mink disease: puzzles and paradigms. Infect Agents Dis 3:279–301PubMedGoogle Scholar
  7. 7.
    Bloom ME, Race RE, Wolfinbarger JB (1980) Characterization of Aleutian diseasevirus as a parvovirus. J Virol 35:836–843PubMedPubMedCentralGoogle Scholar
  8. 8.
    Canuti M, Hugh G, Whitney HG, Lang AS (2015) Amdoparvoviruses in small mammals: expanding our understanding of parvovirus diversity, distribution, and pathology. Front Microbiol 6:1–9CrossRefGoogle Scholar
  9. 9.
    Canuti M, O’Leary KE, Hunter BD, Spearman G, Ojkic D, Whitney HG, Lang AS (2016) Driving forces behind the evolution of the Aleutian mink disease parvovirus in the context of intensive farming. Virus Evol 2:vew004CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Cheng F, Chen AU, Best SM, Bloom ME, Pintel D, Qiu J (2010) The capsid proteins of Aleutian mink disease virus activate caspases and are specifically cleaved during infection. J Virol 84:2687–2696CrossRefPubMedGoogle Scholar
  11. 11.
    Christensen J, Cotmore SF, Tattersall P (1995) Minute virus of mice transcriptional activator protein NS1 binds directly to the transactivation region of the viral P38 promoter in a strictly ATP-dependent manner. J Virol 69:5422–5543PubMedPubMedCentralGoogle Scholar
  12. 12.
    Christensen LS, Gram-Hansen L, Chriél M, Jensen TH (2011) Diversity and stability of Aleutian mink disease virus during bottleneck transitions resulting from eradication in domestic mink in Denmark. Vet Microbiol 149:64–71CrossRefPubMedGoogle Scholar
  13. 13.
    Christensen J, Pedersen M, Aasted B, Alexandersen S (1995) Purification and characterization of the major nonstructural protein (NS-1) of Aleutian mink disease parvovirus. J Virol 69:1802–1809PubMedPubMedCentralGoogle Scholar
  14. 14.
    Clemens DL, Wolfinbarger JB, Mori S, Berry BD, Hayes SF, Bloom ME (1992) Expression of Aleutian mink disease parvovirus capsid proteins by a recombinant vaccinia virus: selfassembly of capsid proteins into particles. J Virol 66:3077–3085PubMedPubMedCentralGoogle Scholar
  15. 15.
    Hahn E, Ramos L, Kenyon AJ (1977) Expression of Aleutian mink disease antigen in cell culture. Infect Immun 15:204–211PubMedPubMedCentralGoogle Scholar
  16. 16.
    Farid AH (2013) Aleutian mink disease virus in furbearing mammals in Nova Scotia,Canada. Acta Vet Scand 55:1–9CrossRefGoogle Scholar
  17. 17.
    Fournier-Chambrillon C, Aasted B, Perrot A, Pontier D, Sauvage F, Artois M, Cassiède J-M, Chauby X, Dal Molin A, Simon C (2004) Antibodies to Aleutianmink disease parvovirus in free-ranging European mink (Mustela lutreola) and other small carnivores from southwestern France. J Wildl Dis 40:394–402CrossRefPubMedGoogle Scholar
  18. 18.
    Gottschalck E, Alexandersen S, Storgaard T, Bloom ME, Aasted B (1994) Sequence comparison of the non-structural genes of four different types of Aleutian mink disease parvovirus indicates an unusual degree of variability. Arch Virol 138:213–231CrossRefPubMedGoogle Scholar
  19. 19.
    Huang Q, Luo Y, Cheng F, Best SM, Bloom ME, Qiu J (2014) Molecular characterization of the small nonstructural proteins of parvovirus Aleutian mink disease virus (AMDV) during infection. Virology 452–453:23–31CrossRefPubMedGoogle Scholar
  20. 20.
    Jepsen JR, Amore F, Baandrup U, Clausen MR, Gottschalck E, Aasted B (2009) Aleutian mink disease virus and humans. Emerg Infect Dis 15:2040–2042CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Li YW, Huang J, Jia Y, Du YJ, Jiang P, Zhang R (2012) Genetic characterization of Aleutian mink disease viruses isolated in China. Virus Genes 45:24–30CrossRefPubMedGoogle Scholar
  22. 22.
    Manas S, Cena JC, Ruiz-Olmo J, Palazón S, Domingo M, Wolfinbarger JB, Bloom ME (2008) Aleutian mink disease parvovirus in wild riparian carnivores in Spain. J Wildl Dis 37:138–144CrossRefGoogle Scholar
  23. 23.
    McKenna R, Olson NH, Chipman PR, Baker TS, Booth TF, Christensen J, Aasted B, Fox JM, Bloom ME, Wolfinbarger JB, Agbandje-McKenna M (1999) Three-dimensional structure of Aleutian mink disease parvovirus: implications for disease pathogenicity. J Virol 73:6882–6891PubMedPubMedCentralGoogle Scholar
  24. 24.
    Mori S, Wolfinbarger JB, Miyazawa M, Bloom ME (1991) Replication of Aleutian mink disease parvovirus in lymphoid tissues of adult mink: involvement of follicular dendritic cells and macrophages. J Virol 65:952–956PubMedPubMedCentralGoogle Scholar
  25. 25.
    Murakami M, Matsuba C, Une Y, Nomura Y, Fujitani H (2001) Nucleotide sequence and polymerase chain reaction/restriction fragment length polymorphism analyses of Aleutian disease virus in ferrets in Japan. J Vet Diagn Investig 13:337–340CrossRefGoogle Scholar
  26. 26.
    Oie KL, Durrant G, Wolfinbarger JB, Martin D, Costello F, Perryman S, Hogan D, Hadlow WJ, Bloom ME (1996) The relationship between capsid protein (VP2) sequence and pathogenicity of Aleutian mink disease parvovirus (ADV): a possible role for raccoons in the transmission of ADV infections. J Virol 70:852–861PubMedPubMedCentralGoogle Scholar
  27. 27.
    Olofsson A, Mittelholzer C, Treiberg Berndtsson L, Lind L, Mejerland T, Belak S (1999) Unusual, high genetic diversity of Aleutian mink disease virus. J Clin Microbiol 37:4145–4149PubMedPubMedCentralGoogle Scholar
  28. 28.
    Porter DD, Larsen AE, Cook NA, Porter HG, Suffin SL (1977) Isolation of Aleutian disease virus of mink in cell culture. Intervirology 8:129–144CrossRefPubMedGoogle Scholar
  29. 29.
    Qiu J, Cheng F, Burger LR, Pintel D (2006) The transcription profile Aleutian mink disease virus in CRFK cells is generated by alternative processing of pre-mRNAs produced from a single promoter. J Virol 80:654–662CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Ryt-Hansen P, Hjulsager CK, Hagberg EE, Chriél M, Struve T, Pedersen AG, Larsen LE (2017) Outbreak tracking of Aleutian mink disease virus (AMDV) using partial NS1 gene sequencing. Virol J 14:119CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Sang Y, Ma J, Hou Z, Zhang Y (2012) Phylogenetic analysis of the VP2 gene ofAleutian mink disease parvoviruses isolated from 2009 to 2011 in China. Virus Genes 45:31–37CrossRefPubMedGoogle Scholar
  32. 32.
    Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Wang ZJ, Wu W, Hu B, Zhang HL, Bai X, Zhao JJ, Zhang L, Yan XJ (2014) Molecular epidemiology of Aleutian mink disease virus in China. Virus Res 184:14–19CrossRefPubMedGoogle Scholar
  34. 34.
    Wu WH, Bloom ME, Berry BD, McGinley MJ, Platt KB (1994) Expression of Aleutian mink disease parvovirus capsid proteins in a baculovirus expression system for potential diagnostic use. J Vet Diagn Investig 6:23–29CrossRefGoogle Scholar
  35. 35.
    Xi J, Wang JG, Yu YL, Zhang XM, Mao YP, Hou Q, Liu WQ (2016) Genetic characterization of the complete genome of an Aleutian mink disease virus isolated in north China. Virus Genes 52:463–473CrossRefPubMedGoogle Scholar
  36. 36.
    Zhang JL, Liu WX, Chen WY, Li CC, Xie MM, Bu ZG (2016) Development of an immuno-peroxidase monolayer assay for the detection of antibodies against peste des petits ruminants virus based on BHK-21 cell line stably expressing the goat signaling lymphocyte activation molecule. PLoS One 11:e0165088CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  • Xue Leng
    • 1
  • Dongxu Liu
    • 2
  • Jianming Li
    • 1
  • Kun Shi
    • 1
  • Fanli Zeng
    • 1
  • Ying Zong
    • 1
  • Yi Liu
    • 1
  • Zhibo Sun
    • 1
  • Shanshan Zhang
    • 1
  • Yadong Liu
    • 1
  • Rui Du
    • 1
  1. 1.College of Chinese Medicine MaterialJilin Agricultural UniversityChangchunPeople’s Republic of China
  2. 2.College of Animal Science and TechnologyJilin Agricultural Science and Technology UniversityJilinPeople’s Republic of China

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