Molecular epidemiological study on Infectious Pancreatic Necrosis Virus isolates from aquafarms in Scotland over three decades Free

Abstract

In order to obtain an insight into genomic changes and associated evolution and adaptation of Infectious Pancreatic Necrosis Virus (IPNV), the complete coding genomes of 57 IPNV isolates collected from Scottish aquafarms from 1982 to 2014 were sequenced and analysed. Phylogenetic analysis of the sequenced IPNV strains showed separate clustering of genogroups I, II, III and V. IPNV isolates with genetic reassortment of segment A/B of genogroup III/II were determined. About 59 % of the IPNV isolates belonged to the persistent type and 32 % to the low-virulent type, and only one highly pathogenic strain (1.79 %) was identified. Codon adaptation index calculations indicated that the IPNV major capsid protein VP2 has adapted to its salmonid host. Under-representation of CpG dinucleotides in the IPNV genome to minimize detection by the innate immunity receptors, and observed positive selection in the virulence determination sites of VP2 embedded in the variable region of the main antigenic region, suggest an immune escape mechanism driving virulence evolution. The prevalence of mostly persistent genotypes, together with the assumption of adaptation and immune escape, indicates that IPNV is evolving with the host.

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2018-10-25
2024-03-28
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References

  1. Munro ES, Midtlyng PJ. Infectious Pancreatic Necrosis and Associated Aquatic Birnaviruses vol. 3 Wallingford, UK: CABI; 2011
    [Google Scholar]
  2. Rønneseth A, Pettersen EF, Wergeland HI. Flow cytometry assay for intracellular detection of Infectious Pancreatic Necrosis virus (IPNV) in Atlantic salmon (Salmo salar L.) leucocytes. Fish Shellfish Immunol 2012; 33:1292–1302 [View Article][PubMed]
    [Google Scholar]
  3. Ahne W, Thomsen I. Infectious pancreatic necrosis: detection of virus and antibodies in rainbow trout IPNV-carrier (Salmo gairdneri). Zentralbl Vet Reihe B 1986; 33:552–554
    [Google Scholar]
  4. Wood EM, Snieszko SF, Yasutake WT. Infectious pancreatic necrosis in brook trout. AMA Arch Pathol 1955; 60:26–28
    [Google Scholar]
  5. Wolf K. Fish Viruses and Fish Virus Diseases Ithaca, NY: Cornell University Press; 1988
    [Google Scholar]
  6. Smail DA, Bruno DW, Dear G, McFarlane LA, Ross K. Infectious pancreatic necrosis (IPN) virus Sp serotype in farmed Atlantic salmon, Salmo salar L., post-smolts associated with mortality and clinical disease. J Fish Dis 1992; 15:77–83 [View Article]
    [Google Scholar]
  7. McKnight IJ, Roberts RJ. The pathology of infectious pancreatic necrosis. I. The sequential histopathology of the naturally ocurring condition. Br Vet J 1976; 132:76–85 [View Article][PubMed]
    [Google Scholar]
  8. Roberts RJ, McKnight IJ. The pathology of infectious pancreatic necrosis. II. Stress-mediated recurrence. Br Vet J 1976; 132:209–214 [View Article][PubMed]
    [Google Scholar]
  9. Wolf K, Dunbar CE, Pyle EA. Infectious pancreatic necrosis of trout: II. Experimental infections with brook trout. The Progressive Fish-Culturist 1961; 23:61–65 [View Article]
    [Google Scholar]
  10. Dobos P. The molecular biology of infectious pancreatic necrosis virus (IPNV). Annu Rev Fish Dis 1995; 5:25–54 [View Article]
    [Google Scholar]
  11. Dobos P. Protein-primed RNA synthesis in vitro by the virion-associated RNA polymerase of infectious pancreatic necrosis virus. Virology 1995; 208:19–25 [View Article][PubMed]
    [Google Scholar]
  12. Duncan R, Dobos P. The nucleotide sequence of infectious pancreatic necrosis virus (IPNV) dsRNA segment A reveals one large ORF encoding a precursor polyprotein. Nucleic Acids Res 1986; 14:5934 [View Article][PubMed]
    [Google Scholar]
  13. Duncan R, Nagy E, Krell PJ, Dobos P. Synthesis of the infectious pancreatic necrosis virus polyprotein, detection of a virus-encoded protease, and fine structure mapping of genome segment A coding regions. J Virol 1987; 61:3655–3664
    [Google Scholar]
  14. Petit S, Lejal N, Huet JC, Delmas B. Active residues and viral substrate cleavage sites of the protease of the birnavirus infectious pancreatic necrosis virus. J Virol 2000; 74:2057–2066 [View Article][PubMed]
    [Google Scholar]
  15. Pedersen T, Skjesol A, Jørgensen JB. VP3, a structural protein of infectious pancreatic necrosis virus, interacts with RNA-dependent RNA polymerase VP1 and with double-stranded RNA. J Virol 2007; 81:6652–6663 [View Article][PubMed]
    [Google Scholar]
  16. Lauksund S, Greiner-Tollersrud L, Chang CJ, Robertsen B. Infectious pancreatic necrosis virus proteins VP2, VP3, VP4 and VP5 antagonize IFNa1 promoter activation while VP1 induces IFNa1. Virus Res 2015; 196:113–121 [View Article][PubMed]
    [Google Scholar]
  17. Hong JR, Gong HY, Wu JL. IPNV VP5, a novel anti-apoptosis gene of the Bcl-2 family, regulates Mcl-1 and viral protein expression. Virology 2002; 295:217–229 [View Article][PubMed]
    [Google Scholar]
  18. Blake S, Ma JY, Caporale DA, Jairath S, Nicholson BL. Phylogenetic relationships of aquatic birnaviruses based on deduced amino acid sequences of genome segment A cDNA. Dis Aquat Organ 2001; 45:89–102 [View Article][PubMed]
    [Google Scholar]
  19. Santi N, Vakharia VN, Evensen Ø. Identification of putative motifs involved in the virulence of infectious pancreatic necrosis virus. Virology 2004; 322:31–40 [View Article][PubMed]
    [Google Scholar]
  20. Song H, Santi N, Evensen O, Vakharia VN. Molecular determinants of infectious pancreatic necrosis virus virulence and cell culture adaptation. J Virol 2005; 79:10289–10299 [View Article][PubMed]
    [Google Scholar]
  21. Mutoloki S, Munang'andu HM, Evensen Ø. Clinical and subclinical forms of infectious pancreatic necrosis virus infections show specific viral genetic fingerprints that link differences in virulence to immunogenicity. Fish Shellfish Immunol 2013; 34:1667 [View Article]
    [Google Scholar]
  22. Hill BJ, Way K. Serological classification of infectious pancreatic necrosis (IPN) virus and other aquatic birnaviruses. Annu Rev Fish Dis 1995; 5:55–77 [View Article]
    [Google Scholar]
  23. Underwood BO, Smale CJ, Brown F, Hill BJ. Relationship of a virus from Tellina tenuis to infectious pancreatic necrosis virus. J Gen Virol 1977; 36:93–109 [View Article][PubMed]
    [Google Scholar]
  24. Zhang CX, Suzuki S. Aquabirnaviruses isolated from marine organisms form a distinct genogroup from other aquabirnaviruses. J Fish Dis 2004; 27:633–643 [View Article][PubMed]
    [Google Scholar]
  25. Dorson M. Vaccination against infectious pancreatic necrosis. In Fish Vaccination London: Academic Press Limited; 1988 pp. 162–171
    [Google Scholar]
  26. Rimstad E. Vaccination against infectious pancreatic necrosis. In Gudding WR, Lillehaug A, Evensen O. (editors) Fish Vaccination Chichester: Wiley & Sons Ltd; 2014 pp. 303–312
    [Google Scholar]
  27. Olsen A, Hellberg H. Fiskehelserapporten 2011. In Olsen AB. (editor) Norwegian Veterinary Institute Oslo: Norwegian Veterinary Institute; 2012
    [Google Scholar]
  28. Ramstad A, Midtlyng PJ. Strong genetic influence on IPN vaccination-and-challenge trials in Atlantic salmon, Salmo salar L. J Fish Dis 2008; 31:567–578 [View Article][PubMed]
    [Google Scholar]
  29. Minitab Inc Minitab reference manual : Macintosh version, release 18 State College, PA: Minitab Inc.; 2010
    [Google Scholar]
  30. Ruane NM, McCleary SJ, McCarthy LJ, Henshilwood K. Phylogenetic analysis of infectious pancreatic necrosis virus in Ireland reveals the spread of a virulent genogroup 5 subtype previously associated with imports. Arch Virol 2015; 160:817–824 [View Article]
    [Google Scholar]
  31. Mutoloki S, Jøssund TB, Ritchie G, Munang'andu HM, Evensen Ø. Infectious pancreatic necrosis virus causing clinical and subclinical infections in Atlantic salmon have different genetic fingerprints. Front Microbiol 2016; 7:1393 [View Article][PubMed]
    [Google Scholar]
  32. Tapia D, Eissler Y, Torres P, Jorquera E, Espinoza JC et al. Detection and phylogenetic analysis of infectious pancreatic necrosis virus in Chile. Dis Aquat Organ 2015; 116:173–184 [View Article]
    [Google Scholar]
  33. Salgado-Miranda C, Rojas-Anaya E, García-Espinosa G, Loza-Rubio E. Molecular characterization of the VP2 gene of infectious pancreatic necrosis virus (IPNV) isolates from Mexico. J Aquat Anim Health 2014; 26:43–51 [View Article][PubMed]
    [Google Scholar]
  34. Bain N, Gregory A, Raynard RS. Genetic analysis of infectious pancreatic necrosis virus from Scotland. J Fish Dis 2008; 31:37–47 [View Article][PubMed]
    [Google Scholar]
  35. Holopainen R, Eriksson-Kallio AM, Gadd T. Molecular characterisation of infectious pancreatic necrosis viruses isolated from farmed fish in Finland. Arch Virol 2017; 162:3459–3471 [View Article]
    [Google Scholar]
  36. Mutoloki S, Evensen O. Sequence similarities of the capsid gene of Chilean and European isolates of infectious pancreatic necrosis virus point towards a common origin. J Gen Virol 2011; 92:1721–1726 [View Article]
    [Google Scholar]
  37. Romero-Brey I, Bandín I, Cutrín JM, Vakharia VN, Dopazo CP. Genetic analysis of aquabirnaviruses isolated from wild fish reveals occurrence of natural reassortment of infectious pancreatic necrosis virus. J Fish Dis 2009; 32:585–595 [View Article][PubMed]
    [Google Scholar]
  38. Moreno P, Olveira JG, Labella A, Cutrín JM, Baro JC et al. Surveillance of viruses in wild fish populations in areas around the Gulf of Cadiz (South Atlantic Iberian Peninsula). Appl Environ Microb 2014
    [Google Scholar]
  39. Wei Y, Li J, Zheng J, Xu H, Li L et al. Genetic reassortment of infectious bursal disease virus in nature. Biochem Biophys Res Commun 2006; 350:277–287 [View Article]
    [Google Scholar]
  40. Wallace IS, McKay P, Murray AG. A historical review of the key bacterial and viral pathogens of Scottish wild fish. J Fish Dis 2017; 40:1741–1756 [View Article]
    [Google Scholar]
  41. Julin K, Johansen LH, Sommer AI, Jørgensen JB. Persistent infections with infectious pancreatic necrosis virus (IPNV) of different virulence in Atlantic salmon, Salmo salar L. J Fish Dis 2015; 38:1005–1019 [View Article][PubMed]
    [Google Scholar]
  42. Ahmadivand S, Soltani M, Behdani M, Evensen Ø, Alirahimi E et al. VP2 (PTA motif) encoding DNA vaccine confers protection against lethal challenge with infectious pancreatic necrosis virus (IPNV) in trout. Mol Immunol 2018; 94:61–67 [View Article][PubMed]
    [Google Scholar]
  43. Moen T, Torgersen J, Santi N, Davidson WS, Baranski M et al. Epithelial Cadherin Determines Resistance to Infectious Pancreatic Necrosis Virus in Atlantic Salmon. Genetics 2015; 200:1313–1326 [View Article]
    [Google Scholar]
  44. Houston RD, Haley CS, Hamilton A, Guy DR, Mota-Velasco JC et al. The susceptibility of Atlantic salmon fry to freshwater infectious pancreatic necrosis is largely explained by a major QTL. Heredity 2010; 105:318–327 [View Article][PubMed]
    [Google Scholar]
  45. Skjesol A, Skjæveland I, Elnæs M, Timmerhaus G, Fredriksen BN et al. IPNV with high and low virulence: host immune responses and viral mutations during infection. Virol J 2011; 8:396 [View Article]
    [Google Scholar]
  46. Gadan K, Sandtrø A, Marjara IS, Santi N, Munang'andu HM et al. Stress-induced reversion to virulence of infectious pancreatic necrosis virus in naïve fry of Atlantic salmon (Salmo salar L.). PLoS One 2013; 8:e54656 [View Article][PubMed]
    [Google Scholar]
  47. Tyagi A, Kumar BTN, Singh NK. Genome dynamics and evolution of codon usage patterns in shrimp viruses. Arch Virol 2017; 162:3137–3142 [View Article]
    [Google Scholar]
  48. Heininger U, Bachtiar NS, Bahri P, Dana A, Dodoo A et al. The concept of vaccination failure. Vaccine 2012; 30:1265–1268 [View Article][PubMed]
    [Google Scholar]
  49. Read AF, Baigent SJ, Powers C, Kgosana LB, Blackwell L et al. Imperfect vaccination can enhance the transmission of highly virulent pathogens. PLoS Biol 2015; 13:e1002198 [View Article]
    [Google Scholar]
  50. Ganusov VV, Antia R. Imperfect vaccines and the evolution of pathogens causing acute infections in vertebrates. Evolution 2006; 60:957–969 [View Article][PubMed]
    [Google Scholar]
  51. Hanada K, Suzuki Y, Gojobori T. A large variation in the rates of synonymous substitution for RNA viruses and its relationship to a diversity of viral infection and transmission modes. Mol Biol Evol 2004; 21:1074–1080 [View Article][PubMed]
    [Google Scholar]
  52. Silva FM, Vidigal PM, Myrrha LW, Fietto JL, Silva A et al. Tracking the molecular epidemiology of Brazilian Infectious bursal disease virus (IBDV) isolates. Infect Genet Evol 2013; 13:18–26 [View Article][PubMed]
    [Google Scholar]
  53. Munro AL, Wallace IS. Scottishfish Farm Production Survey 2016 Edinburgh, UK: Marine Scotland Science; 2017
    [Google Scholar]
  54. Scottish Government 1979-2016; Scottish Fish Farm Production Surveys. www.gov.scot/Topics/marine/Publications/stats/FishFarmProductionSurveys/OlderSurveys
  55. Shwed PS, Dobos P, Cameron LA, Vakharia VN, Duncan R. Birnavirus VP1 proteins form a distinct subgroup of RNA-dependent RNA polymerases lacking a GDD motif. Virology 2002; 296:241–250 [View Article][PubMed]
    [Google Scholar]
  56. Tan DY, Hair Bejo M, Aini I, Omar AR, Goh YM. Base usage and dinucleotide frequency of infectious bursal disease virus. Virus Genes 2004; 28:41–53 [View Article][PubMed]
    [Google Scholar]
  57. Sabath N, Wagner A, Karlin D. Evolution of viral proteins originated de novo by overprinting. Mol Biol Evol 2012; 29:3767–3780 [View Article][PubMed]
    [Google Scholar]
  58. Skjesol A, Aamo T, Hegseth MN, Robertsen B, Jørgensen JB. The interplay between infectious pancreatic necrosis virus (IPNV) and the IFN system: IFN signaling is inhibited by IPNV infection. Virus Res 2009; 143:53–60 [View Article]
    [Google Scholar]
  59. Cheng X, Virk N, Chen W, Ji S, Ji S et al. CpG usage in RNA viruses: data and hypotheses. PLoS One 2013; 8:e74109 [View Article][PubMed]
    [Google Scholar]
  60. Karlin S, Doerfler W, Cardon L. Why is CpG suppressed in the genomes of virtually all small eukaryotic viruses but not in those of large eukaryotic viruses?. J Virol 1994; 68:2889–2897
    [Google Scholar]
  61. Jørgensen JB, Johansen A, Stenersen B, Sommer AI. CpG oligodeoxynucleotides and plasmid DNA stimulate Atlantic salmon (Salmo salar L.) leucocytes to produce supernatants with antiviral activity. Dev Comp Immunol 2001; 25:313–321 [View Article][PubMed]
    [Google Scholar]
  62. Graham SC, Sarin LP, Bahar MW, Myers RA, Stuart DI et al. The N-terminus of the RNA polymerase from infectious pancreatic necrosis virus is the determinant of genome attachment. PLoS Pathog 2011; 7:e1002085 [View Article][PubMed]
    [Google Scholar]
  63. Bahir I, Fromer M, Prat Y, Linial M. Viral adaptation to host: a proteome-based analysis of codon usage and amino acid preferences. Mol Syst Biol 2009; 5:311 [View Article]
    [Google Scholar]
  64. Tello M, Vergara F, Spencer E. Genomic adaptation of the ISA virus to Salmo salar codon usage. Virol J 2013; 10:223 [View Article][PubMed]
    [Google Scholar]
  65. Santi N, Song H, Vakharia VN, Evensen Ø. Infectious pancreatic necrosis virus VP5 is dispensable for virulence and persistence. J Virol 2005; 79:9206–9216 [View Article][PubMed]
    [Google Scholar]
  66. Heppell J, Tarrab E, Berthiaume L, Lecomte J, Arella M. Characterization of the small open reading frame on genome segment A of infectious pancreatic necrosis virus. J Gen Virol 1995; 76:2091–2096 [View Article]
    [Google Scholar]
  67. Weber S, Fichtner D, Mettenleiter TC, Mundt E. Expression of VP5 of infectious pancreatic necrosis virus strain VR299 is initiated at the second in-frame start codon. J Gen Virol 2001; 82:805–812 [View Article]
    [Google Scholar]
  68. Santi N, Sandtrø A, Sindre H, Song H, Hong J-R et al. Infectious pancreatic necrosis virus induces apoptosis in vitro and in vivo independent of VP5 expression. Virology 2005; 342:13–25 [View Article]
    [Google Scholar]
  69. Fryer JL, Yusha A, Pilcher KS. The in vitro cultivation of tissue and cells of Pacific salmon and steelhead trout. Ann N Y Acad Sci 1965; 126:566–586 [View Article][PubMed]
    [Google Scholar]
  70. Wergeland HI, Jakobsen RA. A salmonid cell line (TO) for production of infectious salmon anaemia virus (ISAV). Dis Aquat Organ 2001; 44:183–190 [View Article]
    [Google Scholar]
  71. Officer JE. Ability of a fish cell line to support the growth of mammalian viruses. Proc Soc Exp Biol Med 1964; 116:190–194 [View Article][PubMed]
    [Google Scholar]
  72. Dilcher M, Hasib L, Lechner M, Wieseke N, Middendorf M et al. Genetic characterization of Tribeč virus and Kemerovo virus, two tick-transmitted human-pathogenic Orbiviruses. Virology 2012; 423:68–76 [View Article]
    [Google Scholar]
  73. Schmieder R, Edwards R. Quality control and preprocessing of metagenomic datasets. Bioinformatics 2011; 27:863–864 [View Article]
    [Google Scholar]
  74. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article]
    [Google Scholar]
  75. Schmieder R, Edwards R. Fast identification and removal of sequence contamination from genomic and metagenomic datasets. PLoS One 2011; 6:e17288 [View Article][PubMed]
    [Google Scholar]
  76. Nurk S, Bankevich A, Antipov D, Gurevich AA, Korobeynikov A et al. Assembling single-cell genomes and mini-metagenomes from chimeric MDA products. J Comput Biol 2013; 20:714–737 [View Article][PubMed]
    [Google Scholar]
  77. Thomson E, Ip CL, Badhan A, Christiansen MT, Adamson W et al. Comparison of Next-Generation Sequencing Technologies for Comprehensive Assessment of Full-Length Hepatitis C Viral Genomes. J Clin Microbiol 2016; 54:2470–2484 [View Article][PubMed]
    [Google Scholar]
  78. Lunter G, Goodson M. Stampy: a statistical algorithm for sensitive and fast mapping of Illumina sequence reads. Genome Res 2011; 21:936–939 [View Article][PubMed]
    [Google Scholar]
  79. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [View Article]
    [Google Scholar]
  80. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012; 9:357–359 [View Article]
    [Google Scholar]
  81. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009; 25:2078–2079 [View Article][PubMed]
    [Google Scholar]
  82. Goujon M, McWilliam H, Li W, Valentin F, Squizzato S et al. A new bioinformatics analysis tools framework at EMBL-EBI. Nucleic Acids Res 2010; 38:W695–W699 [View Article][PubMed]
    [Google Scholar]
  83. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K et al. Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 2011; 7:1–6
    [Google Scholar]
  84. Otto TD, Dillon GP, Degrave WS, Berriman M. RATT: Rapid annotation transfer tool. Nucleic Acids Res 2011; 39:e57e57 [View Article][PubMed]
    [Google Scholar]
  85. Kingman JFC. The coalescent. Stoch Proc Appl 1982; 13:235–248 [View Article]
    [Google Scholar]
  86. Kingman JF. On the genealogy of large populations. J Appl Probab 1982; 19:27–43 [View Article]
    [Google Scholar]
  87. Drummond AJ, Suchard MA, Xie D, Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 2012; 29:1969–1973 [View Article][PubMed]
    [Google Scholar]
  88. di Paola N, Freire C, Zanotto P. Does adaptation to vertebrate codon usage relate to flavivirus emergence potential?. PLoS One 2018; 13:e0191652 [View Article][PubMed]
    [Google Scholar]
  89. Puigbò P, Bravo IG, Garcia-Vallvé S. E-CAI: a novel server to estimate an expected value of codon adaptation index (eCAI). BMC Bioinformatics 2008; 9:65 [View Article][PubMed]
    [Google Scholar]
  90. Puigbò P, Bravo IG, Garcia-Vallve S. CAIcal: a combined set of tools to assess codon usage adaptation. Biol Direct 2008; 3:38 [View Article][PubMed]
    [Google Scholar]
  91. Pond SLK, Frost SDW, Muse SV. HyPhy: hypothesis testing using phylogenies. Bioinformatics 2005; 21:676–679 [View Article]
    [Google Scholar]
  92. Rice P, Longden I, Bleasby A. EMBOSS: the European molecular biology open software suite. Trends Genet 2000; 16:276–277 [View Article][PubMed]
    [Google Scholar]
  93. Huson DH, Bryant D. Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 2006; 23:254–267 [View Article][PubMed]
    [Google Scholar]
  94. Glenney GW, Barbash PA, Coll JA, Quartz WM. Isolation and molecular characterization of a novel infectious pancreatic necrosis virus strain in returning Atlantic salmon Salmo salar from the Connecticut River, USA. J Aquat Anim Health 2012; 24:63–72 [View Article][PubMed]
    [Google Scholar]
  95. Mohr PG, Moody NJ, Williams LM, Hoad J, St J Crane M. Molecular characterization of Tasmanian aquabirnaviruses from 1998 to 2013. Dis Aquat Organ 2015; 116:1–9 [View Article][PubMed]
    [Google Scholar]
  96. Cutrin JM, Barja JL, Nicholson BL, Bandin I, Blake S et al. Restriction fragment length polymorphisms and sequence analysis: an approach for genotyping infectious pancreatic necrosis virus reference strains and other aquabirnaviruses isolated from Northwestern Spain. Appl Environ Microbiol 2004; 70:1059–1067 [View Article]
    [Google Scholar]
  97. Dadar M, Peyghan R, Memari HR, Shapouri MR, Hasanzadeh R et al. Sequence analysis of infectious pancreatic necrosis virus isolated from Iranian reared rainbow trout (Oncorhynchus mykiss) in 2012. Virus Genes 2013; 47:574–578 [View Article][PubMed]
    [Google Scholar]
  98. Havarstein LS, Kalland KH, Christie KE, Endresen C. Sequence of the large double-stranded RNA segment of the N1 strain of infectious pancreatic necrosis virus: a comparison with other Birnaviridae. J Gen Virol 1990; 71:299–308 [View Article]
    [Google Scholar]
  99. Heppell J, Berthiaume L, Corbin F, Tarrab E, Lecomte J et al. Comparison of amino acid sequences deduced from a cDNA fragment obtained from infectious pancreatic necrosis virus (IPNV) strains of different serotypes. Virology 1993; 195:840–844 [View Article]
    [Google Scholar]
  100. Chung H, Lee S, Lee H, Lee D, Kim Y. Nucleotide sequence analysis of the VP2-NS-VP3 genes of infectious pancreatic necrosis virus DRT strain. Mol Cells 1993; 4:341–354
    [Google Scholar]
  101. Lee H-H, Chung H-K, Lee S-H. Nucleotide sequence analysis of the RNA-dependent RNA polymerase gene of infectious pancreatic necrosis virus DRT strain. J Microbiol Biotechn 1994; 4:264–269
    [Google Scholar]
  102. Yao K, Vakharia VN. Generation of infectious pancreatic necrosis virus from cloned cDNA. J Virol 1998; 72:8913–8920
    [Google Scholar]
  103. Hirayama T, Nagano I, Shinmoto H, Yagyu K, Oshima S. Isolation and characterization of virulent yellowtail ascites virus. Microbiol Immunol 2007; 51:397–406 [View Article][PubMed]
    [Google Scholar]
  104. Zhao Z, Ke F, Li Z, Gui J, Zhang Q. Isolation, characterization and genome sequence of a birnavirus strain from flounder Paralichthys olivaceus in China. Arch Virol 2008; 153:1143–1148 [View Article][PubMed]
    [Google Scholar]
  105. Zhang CX, Suzuki S. Comparison of the RNA polymerase genes of marine birnavirus strains and other birnaviruses. Arch Virol 2003; 148:745–758 [View Article][PubMed]
    [Google Scholar]
  106. Bandín I, Souto S, Cutrín JM, López-Vázquez C, Olveira JG et al. Presence of viruses in wild eels Anguilla anguilla L, from the Albufera Lake (Spain). J Fish Dis 2014; 37:597–607 [View Article][PubMed]
    [Google Scholar]
  107. Galloux M, Chevalier C, Henry C, Huet JC, Costa BD et al. Peptides resulting from the pVP2 C-terminal processing are present in infectious pancreatic necrosis virus particles. J Gen Virol 2004; 85:2231–2236 [View Article][PubMed]
    [Google Scholar]
  108. Dixon PF, Ngoh GH, Stone DM, Chang SF, Way K et al. Proposal for a fourth aquabirnavirus serogroup. Arch Virol 2008; 153:1937–1941 [View Article][PubMed]
    [Google Scholar]
  109. Duncan R, Mason CL, Nagy E, Leong JA, Dobos P. Sequence analysis of infectious pancreatic necrosis virus genome segment B and its encoded VP1 protein: a putative RNA-dependent RNA polymerase lacking the Gly-Asp-Asp motif. Virology 1991; 181:541–552 [View Article][PubMed]
    [Google Scholar]
  110. Shivappa RB, Song H, Yao K, Aas-Eng A, Evensen O et al. Molecular characterization of Sp serotype strains of infectious pancreatic necrosis virus exhibiting differences in virulence. Dis Aquat Organ 2004; 61:23–32 [View Article][PubMed]
    [Google Scholar]
  111. Jorquera E, Morales P, Tapia D, Torres P, Eissler Y et al. Chilean IPNV isolates: Robustness analysis of PCR detection. Electronic J Biotechnol 2016; 19:28–32
    [Google Scholar]
  112. Nobiron I, Galloux M, Henry C, Torhy C, Boudinot P et al. Genome and polypeptides characterization of Tellina virus 1 reveals a fifth genetic cluster in the Birnaviridae family. Virology 2008; 371:350–361 [View Article][PubMed]
    [Google Scholar]
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