Novel Atlantic bottlenose dolphin parainfluenza virus TtPIV-1 clusters with bovine PIV-3 genotype B strains

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Abstract

Parainfluenza virus 3 (PIV-3) is a common viral infection not only in humans, but also in many other species. Serological evidence suggests that nearly 100 % of children in the United States have been infected with PIV-3 by 5 years of age. Similarly, in cattle, PIV-3 is commonly associated with bovine respiratory disease complex. A novel dolphin PIV-3 (TtPIV-1) was described by Nollens et al. in 2008 from a dolphin that was diagnosed with an unknown respiratory illness. At that time, TtPIV-1 was found to be most similar to, but distinct from, bovine PIV-3 (BPIV-3). In the present study, similar viral growth kinetics and pro-inflammatory cytokine (IL-1β, IL-6, and CXCL8) production were seen between BPIV-3 and TtPIV-1 in BEAS-2B, MDBK, and Vero cell lines. Initial nomenclature of TtPIV-1 was based on partial sequence of the fusion and RNA polymerase genes. Based on the similarities we saw with the in vitro work, it was important to examine the TtPIV-1 genome in more detail. Full genome sequencing and subsequent phylogenetic analysis revealed that all six viral genes of TtPIV-1 clustered within the recently described BPIV-3 genotype B strains, and it is proposed that TtPIV-1 be re-classified with BPIV-3 genotype B strains.

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References

  1. 1.

    A. Chang, R.E. Dutch, Viruses 4, 613–636 (2012)

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  2. 2.

    J.S. Tregoning, J. Schwarze, Clin. Microbiol. Rev. 23, 74–98 (2010)

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  3. 3.

    R.E. El Feghaly, L. McGann, C.A. Bonville, P.J. Branigan, M. Suryadevera, H.F. Rosenberg, J.B. Domachowske, Pediatr. Infect. Dis. J. 29, e26 (2010)

    PubMed Central  PubMed  Google Scholar 

  4. 4.

    S.S. Maidana, P.M. Lomonaco, G. Combessies, M.I. Craig, J. Diodati, D. Rodriguez, V. Parreño, O. Zabal, J.L. Konrad, G. Crudelli, BMC Vet. Res. 8, 83–91 (2012)

    PubMed Central  Article  PubMed  Google Scholar 

  5. 5.

    R. Kasimanickam, Bovine Respiratory Disease “Shipping Fever” in Cattle. (Washington State University, 2010), http://extension.wsu.edu/vetextension/Beef/Documents/BovineRespiratoryDisease_Aug2010.pdf. Accessed 10 Apr 2015

  6. 6.

    H.H. Nollens, J.F. Wellehan, J.T. Saliki, S.L. Caseltine, E.D. Jensen, W. Van Bonn, S. Venn-Watson, Vet. Microbiol. 128, 231–242 (2008)

    CAS  Article  PubMed  Google Scholar 

  7. 7.

    S. Venn-Watson, R. Rivera, C.R. Smith, J.T. Saliki, S. Caseltine, J.St Leger, P. Yochem, R.S. Wells, H. Nollens, Emerging Infect. Dis. 14, 397–405 (2008)

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  8. 8.

    H. Kimura, M. Yoshizumi, H. Ishii, K. Oishi, A. Ryo, Front. Microbiol. 4, 276–284 (2013)

    PubMed Central  Article  PubMed  Google Scholar 

  9. 9.

    M. Vareille, E. Kieninger, M.R. Edwards, N. Regamey, Clin. Microbiol. Rev. 24, 210–229 (2011)

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  10. 10.

    C.A. Dinarello, Chest 118, 503–508 (2000)

    CAS  Article  PubMed  Google Scholar 

  11. 11.

    J. Scheller, A. Chalaris, D. Schmidt-Arras, S. Rose-John, Biochem. Biophys. Acta 1813, 878–888 (2011)

    CAS  Article  PubMed  Google Scholar 

  12. 12.

    T. Roger, P. Bresser, M. Snoek, K. van der Sluijs, A. van den Berg, M. Nijhuis, H.M. Jansen, R. Lutter, Am. J. Physiol. Lung Cell. Mol. Physiol. 287, L1048–L1055 (2004)

    CAS  Article  PubMed  Google Scholar 

  13. 13.

    P.S. McNamara, B.F. Flanagan, C.A. Hart, R.L. Smyth, J. Infect. Dis. 191, 1225–1232 (2005)

    CAS  Article  PubMed  Google Scholar 

  14. 14.

    M. Breindahl, K. Rieneck, C. Nielsen, T. Justesen, K. Bendtzen, K. Müller, Open J. of Immunol. 2, 40–48 (2012)

    CAS  Article  Google Scholar 

  15. 15.

    R. Levitz, R. Wattier, P. Phillips, A. Solomon, J. Lawler, I. Lazar, C. Weibel, J.S. Kahn, Virol. J. 9, 190–198 (2012)

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  16. 16.

    K. Childs, N. Stock, C. Ross, J. Andrejeva, L. Hilton, M. Skinner, R. Randall, S. Goodbourn, Virology 359, 190–200 (2007)

    CAS  Article  PubMed  Google Scholar 

  17. 17.

    K.J. Livak, T.D. Schmittgen, Methods 25, 402–408 (2001)

    CAS  Article  PubMed  Google Scholar 

  18. 18.

    J.L. McGill, R.E. Sacco, C.L. Baldwin, J.C. Telfer, M.V. Palmer, W.R. Waters, J. Immunol. 192, 2756–2769 (2014)

    CAS  Article  PubMed  Google Scholar 

  19. 19.

    L.J. Reed, H. Muench, J. Hyg. 27, 493–497 (1938)

    Google Scholar 

  20. 20.

    J.D. Neill, D.O. Bayles, J.F. Ridpath, J. Virol. Methods 201, 68–72 (2014)

    CAS  Article  PubMed  Google Scholar 

  21. 21.

    N. Elango, Virus Res. 12, 77–86 (1989)

    CAS  Article  PubMed  Google Scholar 

  22. 22.

    Á. Sánchez, A.K. Banerjee, Y. Furuichi, M.A. Richardson, Virology 152, 171–180 (1986)

    Article  PubMed  Google Scholar 

  23. 23.

    A.G. Malur, S.K. Choudhary, B.P. De, A.K. Banerjee, J. Virol. 76, 8101–8109 (2002)

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  24. 24.

    M. Kawano, H. Bando, S. Ohgimoto, K. Okamoto, K. Kondo, M. Tsurudome, M. Nishio, Y. Ito, Virology 179, 857–861 (1990)

    CAS  Article  PubMed  Google Scholar 

  25. 25.

    A.E. Gardner, K.L. Martin, R.E. Dutch, Biochemistry 46, 5094–5105 (2007)

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  26. 26.

    A.E. Gardner, R.E. Dutch, J. Virol. 81, 8303–8314 (2007)

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  27. 27.

    L. Wang, B.H. Harcourt, M. Yu, A. Tamin, P.A. Rota, W.J. Bellini, B.T. Eaton, Microbes Infect. 3, 279–287 (2001)

    CAS  Article  PubMed  Google Scholar 

  28. 28.

    C.J. Russell, T.S. Jardetzky, R.A. Lamb, J. Virol. 78, 13727–13742 (2004)

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  29. 29.

    J. Stone-Hulslander, T.G. Morrison, J. Virol. 73, 3630–3637 (1999)

    PubMed Central  CAS  PubMed  Google Scholar 

  30. 30.

    G. Santos-López, T. Scior, M.D.T. Borraz-Argüello, V. Vallejo-Ruiz, I. Herrera-Camacho, J. Tapia-Ramírez, J. Reyes-Leyva, Braz. J. Infect. Dis. 13, 24–34 (2009)

    Google Scholar 

  31. 31.

    K.J. Henrickson, Clin. Microbiol. Rev. 16, 242–264 (2003)

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  32. 32.

    Z. Dinter, D. Morein, (eds.), Virus Infections in Ruminants (Elsevier Science Publishers BV, New York, 1990)

  33. 33.

    J.M. Emeny, M.J. Morgan, J. Gen. Virol. 43, 247–252 (1979)

    CAS  Article  PubMed  Google Scholar 

  34. 34.

    J. Andrejeva, K.S. Childs, D.F. Young, T.S. Carlos, N. Stock, S. Goodbourn, R.E. Randall, Proc. Natl. Acad. Sci. U.S.A. 101, 17264–17269 (2004)

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  35. 35.

    L.L. Lu, M. Puri, C.M. Horvath, G.C. Sen, J. Biol. Chem. 283, 14269–14276 (2008)

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  36. 36.

    K.S. Childs, J. Andrejeva, R.E. Randall, S. Goodbourn, J. Virol. 83, 1465–1473 (2009)

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  37. 37.

    K. Childs, R. Randall, S. Goodbourn, J. Virol. 86, 3411–3421 (2012)

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  38. 38.

    Y. Kitagawa, M. Yamaguchi, M. Zhou, M. Nishio, M. Itoh, B. Gotoh, J. Virol. 87, 7966–7976 (2013)

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  39. 39.

    M. Yamaguchi, Y. Kitagawa, M. Zhou, M. Itoh, B. Gotoh, FEBS Lett. 588, 28–34 (2014)

    CAS  Article  PubMed  Google Scholar 

  40. 40.

    T.M. Kuo, C.P. Hu, Y.L. Chen, M.H. Hong, K.S. Jeng, C.C.T. Liang, M.L. Chen, C. Chang, J. Biomed. Sci. 16, 41–49 (2009)

    PubMed Central  Article  PubMed  Google Scholar 

  41. 41.

    M.Á.G. Morales, C.C. Gutiérrez, F.M. Nepomuceno, L.V. Peralta, E.V. Maqueda, M.E.M. Zavala, J. Immunol. Res. 2014, 515984–515995 (2014)

    Google Scholar 

  42. 42.

    V.A. Young, G.G. Parks, J. Virol. 77, 7124–7130 (2003)

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  43. 43.

    R.C. Reisinger, K.L. Heddleston, C.A. Manthei, J. Am. Vet. Med. Assoc. 135, 147–152 (1959)

    CAS  PubMed  Google Scholar 

  44. 44.

    A.B. Hoerlein, M.E. Mansfield, F.R. Abinanti, R.J. Huebner, J. Am. Vet. Med. Assoc. 135, 153–160 (1959)

    CAS  PubMed  Google Scholar 

  45. 45.

    J.A. Ellis, Vet. Clin. North Am. Food Anim. Pract. 26, 575–593 (2010)

    Article  PubMed  Google Scholar 

  46. 46.

    P.F. Horwood, J.L. Gravel, T.J. Mahony, J. Gen. Virol. 89, 1643–1648 (2008)

    CAS  Article  PubMed  Google Scholar 

  47. 47.

    Y.M. Zhu, H.F. Shi, Y.R. Gao, J.Q. Xin, N.H. Liu, W.H. Xiang, X.G. Ren, J.K. Feng, L.P. Zhao, F. Xue, Vet. Microbiol. 149, 446–451 (2011)

    CAS  Article  PubMed  Google Scholar 

  48. 48.

    J.K. Oem, E.Y. Lee, K.K. Lee, S.H. Kim, M.H. Lee, B.H. Hyun, Vet. Microbiol. 162, 224–227 (2013)

    CAS  Article  PubMed  Google Scholar 

  49. 49.

    J.D. Neill, J.F. Ridpath, B.T. Valayudhan, BMC Vet. Res. 11, 112 (2015)

    Article  Google Scholar 

  50. 50.

    T. Komatsu, K. Takeuchi, B. Gotoh, Microbes and Infect. 9, 954–962 (2007)

    CAS  Article  Google Scholar 

  51. 51.

    Z. Ben-Ishai, V. Naftali, A. Avram, S. Yatziv, J. Med. Virol. 6, 165–168 (1980)

    CAS  Article  PubMed  Google Scholar 

  52. 52.

    P. Boeuf, I. Vigan-Womas, D. Jublot, S. Loizon, J.C. Barale, B.D. Akanmori, O. Mercereau-Puijalon, C. Behr, BMC Immunol. 6, 5–18 (2005)

    PubMed Central  Article  PubMed  Google Scholar 

  53. 53.

    R.E. Sacco, B.J. Nonnecke, M.V. Palmer, W.R. Waters, J.D. Lippolis, T.A. Reinhardt, PLoS ONE 7, e33074 (2012)

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  54. 54.

    A. Hinzey, J. Alexander, J. Corry, K.M. Adams, A.M. Claggett, Z.P. Traylor, I.C. Davis, J.I. Webster, Marketon. Endocrinology 152, 483–494 (2011)

    PubMed Central  CAS  Article  PubMed  Google Scholar 

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Acknowledgments

We thank James Wellehan at the University of Florida Marine Mammal Health Program for providing us the TtPIV-1 isolate. We would also like to thank Judith Stasko in the Microscopy Services Unit at the National Animal Disease Center, Ames, IA for help with the electron microscopy portion. Funding for this project was supported in part by the Office of Naval Research Grant N0001412IP20029.

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Correspondence to Randy E. Sacco.

Additional information

The GenBank Accession Number for the complete genome of TtPIV-1 is KP764763.

Edited by William Dundon.

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Eberle, K.C., Neill, J.D., Venn-Watson, S.K. et al. Novel Atlantic bottlenose dolphin parainfluenza virus TtPIV-1 clusters with bovine PIV-3 genotype B strains. Virus Genes 51, 198–208 (2015). https://doi.org/10.1007/s11262-015-1224-7

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Keywords

  • Parainfluenza virus
  • Epithelial cells
  • Real-time PCR
  • Phylogeny
  • Growth kinetics
  • Pro-inflammatory cytokines