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Genomic and evolutionary characterization of a novel influenza-C-like virus from swine

Archives of Virology volume 159, pages 249–255 (2014)Cite this article

Abstract

We recently described the isolation of a novel influenza virus from swine exhibiting respiratory disease in the United States that is distantly related to human influenza C virus. Based on genetic, biochemical and morphological analysis, the virus was provisionally classified as C/swine/Oklahoma/1334/2011 (C/OK). To further understand the genetics and evolution of this novel pathogen, we performed a comprehensive analysis of its sequence and phylogeny. The results demonstrated that C/OK and human influenza C viruses share a conserved array of predicted functional domains in the viral RNA genome replication and viral entry machinery but vary at key functional sites. Furthermore, our evolutionary analysis showed that homologous genes of C/OK and human influenza C viruses diverged from each other an estimated several hundred to several thousand years ago. Taken together, the findings described in this study support and extend our previous observations that C/OK is a genetically and evolutionarily distinct influenza virus in the family Orthomyxoviridae.

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References

  1. Boivin S, Cusack S, Ruigrok RWH, Hart DJ (2010) Influenza A virus polymerase: structural insights into replication and host adaptation mechanisms. J Biol Chem 285:28411–28417

    CAS  PubMed  Article  Google Scholar 

  2. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214

    PubMed Central  PubMed  Article  Google Scholar 

  3. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  4. Eisenberg D, Luthy R, Bowie JU (1997) VERIFY3D: assessment of protein models with three-dimensional profiles. Methods Enzymol 277:396–404

    CAS  PubMed  Article  Google Scholar 

  5. Eswar N, Webb B, Marti-Renom MA, Madhusudhan MS, Eramian D, Shen MY, Pieper U, Sali A (2007) Comparative protein structure modeling using MODELLER. Curr Protoc Protein Sci. Chapter 2: Unit 2.9

  6. Gambaryan AS, Marinina VP, Tuzikov AB, Bovin NV, Rudneva IA, Sinitsyn BV, Shilov AA, Matrosovich MN (1998) Effects of host-dependent glycosylation of hemagglutinin on receptor-binding properties on H1N1 human influenza A virus grown in MDCK cells and in embryonated eggs. Virology 247:170–177

    CAS  PubMed  Article  Google Scholar 

  7. Gatherer D (2010) Tempo and mode in the molecular evolution of influenza C. PLoS Curr 2:RRN1199

    Google Scholar 

  8. Guilligay D, Tarendeau F, Resa-Infante P, Coloma R, Crepin T, Sehr P, Lewis J, Ruigrok RW, Ortin J, Hart DJ, Cusack S (2008) The structural basis for cap binding by influenza virus polymerase subunit PB2. Nat Struct Mol Biol 15:500–506

    CAS  PubMed  Article  Google Scholar 

  9. Guo YJ, Jin FG, Wang P, Wang M, Zhu JM (1983) Isolation of influenza C virus from pigs and experimental infection of pigs with influenza C virus. J Gen Virol 64(Pt 1):177–182

    PubMed  Google Scholar 

  10. Hause BM, Ducatez M, Collin EA, Ran Z, Liu R, Sheng Z, Armien A, Kaplan B, Chakravarty S, Hoppe AD, Webby RJ, Simonson RR, Li F (2013) Isolation of a Novel Swine Influenza Virus from Oklahoma in 2011 Which Is Distantly Related to Human Influenza C Viruses. PLoS pathog 9:e1003176

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  11. He XJ, Zhou J, Bartlam M, Zhang RG, Ma JY, Lou ZY, Li XM, Li JJ, Joachimiak A, Zeng ZH, Ge RW, Rao ZH, Liu YF (2008) Crystal structure of the polymerase PA(C)-PB1(N) complex from an avian influenza H5N1 virus. Nature 454:1123–1126

    CAS  PubMed  Article  Google Scholar 

  12. Ito T, Kawaoka Y, Vines A, Ishikawa H, Asai T, Kida H (1998) Continued circulation of reassortant H1N2 influenza viruses in pigs in Japan. Arch Virol 143:1773–1782

    CAS  PubMed  Article  Google Scholar 

  13. Kall L, Krogh A, Sonnhammer EL (2004) A combined transmembrane topology and signal peptide prediction method. J Mol Biol 338:1027–1036

    CAS  PubMed  Article  Google Scholar 

  14. Krogh A, Larsson B, von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580

    CAS  PubMed  Article  Google Scholar 

  15. Osterhaus ADME, Rimmelzwaan GF, Martina BEE, Bestebroer TM, Fouchier RAM (2000) Influenza B virus in seals. Science 288:1051–1053

    CAS  PubMed  Article  Google Scholar 

  16. Palese PSM (2007) Orthomyxoviridae: The viruses and their replication. In: Knipe DM, Howley PM (eds) Fields Virology, 5th edn. Lippincott Williams & Wilkins, Philadelphia, pp 1647–1690

    Google Scholar 

  17. Pease CM (1987) An evolutionary epidemiological mechanism, with applications to type A influenza. Theor Popul Biol 31:422–452

    CAS  PubMed  Article  Google Scholar 

  18. Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8:785–786

    CAS  PubMed  Article  Google Scholar 

  19. Poeppl W, Hell M, Herkner H, Stoiser B, Fritsche G, Schurz-Bamieh N, Poeppl G, Gattringer R, Jones N, Maass M, Egle A, Burgmann H (2011) Clinical aspects of 2009 pandemic influenza A (H1N1) virus infection in Austria. Infection 39:341–352

    CAS  PubMed  Article  Google Scholar 

  20. Pond SLK, Posada D, Gravenor MB, Woelk CH, Frost SDW (2006) Automated phylogenetic detection of recombination using a genetic algorithm. Mol Biol Evol 23:1891–1901

    CAS  Article  Google Scholar 

  21. Schulze IT (1997) Effects of glycosylation on the properties and functions of influenza virus hemagglutinin. J Infect Dis 176(Suppl 1):S24–S28

    PubMed  Article  Google Scholar 

  22. Sun SS, Wang QZ, Zhao F, Chen WT, Li Z (2011) Glycosylation Site Alteration in the Evolution of Influenza A (H1N1) Viruses. PLoS One 6(7):e22844

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  23. Szepanski S, Veit M, Pleschka S, Klenk HD, Schmidt MF, Herrler G (1994) Post-translational folding of the influenza C virus glycoprotein HEF: defective processing in cells expressing the cloned gene. J Gen Virol 75(Pt 5):1023–1030

    CAS  PubMed  Article  Google Scholar 

  24. Takashita E, Muraki Y, Sugawara K, Asao H, Nishimura H, Suzuki K, Tsuji T, Hongo S, Ohara Y, Kawaoka Y, Ozawa M, Matsuzaki Y (2012) Intrinsic temperature sensitivity of influenza C virus hemagglutinin-esterase-fusion protein. J Virol 86:13108–13111

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  25. 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 28:2731–2739

    CAS  PubMed  Article  Google Scholar 

  26. Tarendeau F, Boudet J, Guilligay D, Mas PJ, Bougault CM, Boulo S, Baudin F, Ruigrok RWH, Daigle N, Ellenberg J, Cusack S, Simorre JP, Hart DJ (2007) Structure and nuclear import function of the C-terminal domain of influenza virus polymerase PB2 subunit. Nat Struct Mol Biol 14:229–233

    CAS  PubMed  Article  Google Scholar 

  27. Tong S, Li Y, Rivailler P, Conrardy C, Castillo DA, Chen LM, Recuenco S, Ellison JA, Davis CT, York IA, Turmelle AS, Moran D, Rogers S, Shi M, Tao Y, Weil MR, Tang K, Rowe LA, Sammons S, Xu X, Frace M, Lindblade KA, Cox NJ, Anderson LJ, Rupprecht CE, Donis RO (2012) A distinct lineage of influenza A virus from bats. Proc Natl Acad Sci USA 109(11):4269–4274

    CAS  PubMed  Article  Google Scholar 

  28. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y (1992) Evolution and ecology of influenza A viruses. Microbiol Rev 56:152–179

    CAS  PubMed Central  PubMed  Google Scholar 

  29. Yamashita M, Krystal M, Fitch WM, Palese P (1988) Influenza B virus evolution: co-circulating lineages and comparison of evolutionary pattern with those of influenza A and C viruses. Virology 163:112–122

    CAS  PubMed  Article  Google Scholar 

  30. Yuan PW, Bartlam M, Lou ZY, Chen SD, Zhou J, He XJ, Lv ZY, Ge RW, Li XM, Deng T, Fodor E, Rao ZH, Liu YF (2009) Crystal structure of an avian influenza polymerase PA(N) reveals an endonuclease active site. Nature 458:909–913

    CAS  PubMed  Article  Google Scholar 

Download references

Acknowledgments

This research was supported in part by the SDSU AES Fund 3AH203, a Public Health Service grant (AI076125 to F.L.), and SD 2010 Research Center (Biological Control and Analysis of Applied Photonics, BCAAP) Fund (3SJ163 to F.L.). Research in the S.C. laboratory is supported by the SDSU AES to S.C. and the South Dakota 2010 Research Center, BCAAP (Biological Control and Analysis of Applied Photonics) Fund (3SG163 to S.C.).

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Authors and Affiliations

  1. Department of Chemistry and Biochemistry, South Dakota State University, Brookings, SD, 57007, USA

    Zizhang Sheng, Adam D. Hoppe & Suvobrata Chakravarty

  2. Department of Veterinary and Biomedical Sciences, South Dakota State University, Brookings, SD, 57007, USA

    Zhiguang Ran, Ben M. Hause & Feng Li

  3. Department of Biology and Microbiology, South Dakota State University, Brookings, SD, 57007, USA

    Zhiguang Ran & Feng Li

  4. Department of Health and Nutrition Sciences, South Dakota State University, Brookings, SD, 57007, USA

    Dan Wang

  5. Newport Laboratories, Worthington, MN, 56187, USA

    Randy Simonson & Ben M. Hause

  6. Shandong Poultry Institute, Shandong Academy of Agricultural Sciences, Jinan, 250023, China

    Feng Li

Authors
  1. Zizhang Sheng
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  2. Zhiguang Ran
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  3. Dan Wang
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  4. Adam D. Hoppe
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  5. Randy Simonson
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  6. Suvobrata Chakravarty
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  7. Ben M. Hause
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  8. Feng Li
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Corresponding authors

Correspondence to Suvobrata Chakravarty or Feng Li.

Additional information

Z. Sheng and Z. Ran contributed equally to this work.

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Sheng, Z., Ran, Z., Wang, D. et al. Genomic and evolutionary characterization of a novel influenza-C-like virus from swine. Arch Virol 159, 249–255 (2014). https://doi.org/10.1007/s00705-013-1815-3

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  • DOI: https://doi.org/10.1007/s00705-013-1815-3

Keywords

  • Influenza
  • Influenza Virus
  • Glycosylation Site
  • Human Influenza
  • High Posterior Density