Skip to main content
Springer Nature Link
Log in

Changes in nonstructural protein 3 are associated with attenuation in avian coronavirus infectious bronchitis virus

  • Published:
Virus Genes Aims and scope Submit manuscript

Abstract

Full-length genome sequencing of pathogenic and attenuated (for chickens) avian coronavirus infectious bronchitis virus (IBV) strains of the same serotype was conducted to identify genetic differences between the pathotypes. Analysis of the consensus full-length genome for three different IBV serotypes (Ark, GA98, and Mass41) showed that passage in embryonated eggs, to attenuate the viruses for chickens, resulted in 34.75–43.66% of all the amino acid changes occurring in nsp 3 within a virus type, whereas changes in the spike glycoprotein, thought to be the most variable protein in IBV, ranged from 5.8 to 13.4% of all changes. The attenuated viruses did not cause any clinical signs of disease and had lower replication rates than the pathogenic viruses of the same serotype in chickens. However, both attenuated and pathogenic viruses of the same serotype replicated similarly in embryonated eggs, suggesting that mutations in nsp 3, which is involved in replication of the virus, might play an important role in the reduced replication observed in chickens leading to the attenuated phenotype.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+
from $39.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Explore related subjects

Discover the latest articles, books and news in related subjects, suggested using machine learning.

Abbreviations

IBV:

Infectious bronchitis virus

RTC:

Replication transcription complex

PLP:

Papain-like protease

References

  1. S.P. Mondal, C.J. Cardona, Virology 324, 238–248 (2004)

    Article  PubMed  CAS  Google Scholar 

  2. D. Cavanagh, Vet. Res. 38, 281–297 (2007)

    Article  PubMed  CAS  Google Scholar 

  3. P.C. Woo, S.K. Lau, C.S. Lam, K.K. Lai, Y. Huang, P. Lee, G.S. Luk, K.C. Dyrting, K.H. Chan, K.Y. Yuen, J. Virol. 83, 908–917 (2009)

    Article  PubMed  CAS  Google Scholar 

  4. K.P. Lim, D.X. Liu, J. Biol. Chem. 276, 17515–17523 (2001)

    Article  PubMed  CAS  Google Scholar 

  5. D. Cavanagh, J. Gelb Jr, Infectioius bronchitis, in Diseases of poultry, ed. by Y.M. Saif, A.M. Fadley, J.R. Glisson, L.R. McDougald, L.K. Nolan, D.E. Swayne (Blackwell Publishing, Ames, 2008), pp. 117–135

    Google Scholar 

  6. G. Koch, A. Kant, J.K.A. Cook, D. Cavanagh, Epitopes of neutralizing antibodies are located within three regions of the S1 spike protein of infectious bronchitis virus, in II. International symposium on infectious bronchitis, ed. by E.F. Kaleta, U. Heffels-Redmann (World Veterinary Poultry Association, Rauischholzhausen, 1991), pp. 154–160

    Google Scholar 

  7. A. Kant, G. Koch, D.J. van Roozelaar, J.G. Kusters, F.A. Poelwijk, B.A. van der Zeijst, J. Gen. Virol. 73, 591–596 (1992)

    Article  PubMed  CAS  Google Scholar 

  8. K.M. Moore, M.W. Jackwood, D.A. Hilt, Arch. Virol. 142, 2249–2256 (1997)

    Article  PubMed  CAS  Google Scholar 

  9. I. Imbert, E.J. Snijder, M. Dimitrova, J.C. Guillemot, P. Lecine, B. Canard, Virus Res. 133, 136–148 (2008)

    Article  PubMed  CAS  Google Scholar 

  10. M.J. van Hemert, S.H. van den Worm, K. Knoops, A.M. Mommaas, A.E. Gorbalenya, E.J. Snijder, PLoS Pathol. 4, e1000054 (2008)

    Article  Google Scholar 

  11. J. Ziebuhr, V. Thiel, A.E. Gorbalenya, J. Biol. Chem. 276, 33220–33232 (2001)

    Article  PubMed  CAS  Google Scholar 

  12. S.G. Fang, H. Shen, J. Wang, F.P. Tay, D.X. Liu, Virology 379, 175–180 (2008)

    Article  PubMed  CAS  Google Scholar 

  13. M. Oostra, E.G. te Lintelo, M. Deijs, M.H. Verheije, P.J. Rottier, C.A. de Haan, J. Virol. 81, 12323–12336 (2007)

    Article  PubMed  CAS  Google Scholar 

  14. L. Li, C. Xue, F. Chen, J. Qin, Q. Xie, Y. Bi, Y. Cao, Vet. Microbiol. 143, 145–154 (2010)

    Article  PubMed  CAS  Google Scholar 

  15. M. Oostra, M.C. Hagemeijer, M. van Gent, C.P. Bekker, E.G. te Lintelo, P.J. Rottier, C.A. de Haan, J. Virol. 82, 12392–12405 (2008)

    Article  PubMed  CAS  Google Scholar 

  16. R.L. Graham, J.S. Sparks, L.D. Eckerle, A.C. Sims, M.R. Denison, Virus Res. 133, 88–100 (2008)

    Article  PubMed  CAS  Google Scholar 

  17. M.M. Cao, H. Ren, P. Zhao, W. Pan, Q.L. Chen, Z.T. Qi, J. Virol. Methods 157, 168–174 (2009)

    Article  PubMed  CAS  Google Scholar 

  18. Y.P. Huang, C.H. Wang, Avian Pathol 36, 59–67 (2007)

    Article  PubMed  CAS  Google Scholar 

  19. S. Liu, Z. Han, J. Chen, X. Liu, Y. Shao, X. Kong, G. Tong, J. Rong, Avian Pathol 36, 231–234 (2007)

    Article  PubMed  CAS  Google Scholar 

  20. T. Hodgson, R. Casais, B. Dove, P. Britton, D. Cavanagh, J. Virol. 78, 13804–13811 (2004)

    Article  PubMed  CAS  Google Scholar 

  21. M. Armesto, D. Cavanagh, P. Britton, PLoS One 4, e7384 (2009)

    Article  PubMed  Google Scholar 

  22. A. Ammayappan, C. Upadhyay, J. Gelb Jr, V.N. Vakharia, Arch. Virol. 154, 495–499 (2009)

    Article  PubMed  CAS  Google Scholar 

  23. C.W. Lee, M.W. Jackwood, Virus Res. 80, 33–39 (2001)

    Article  PubMed  CAS  Google Scholar 

  24. J.J. Gelb, M.W. Jackwood, Infectious bronchitis, in A laboratory manual for the isolation, identification, and characterization of Avian pathogens, ed. by L. Dufour-Zavala, D.E. Swayne, J.R. Glisson, J.E. Pearson, W.M. Reed, M.W. Jackwood, P. Woolcock (American Association of Avian Pathologists, Kennett Square, 2008), pp. 146–149

    Google Scholar 

  25. M.W. Jackwood, T.O. Boynton, D.A. Hilt, E.T. McKinley, J.C. Kissinger, A.H. Paterson, J. Robertson, C. Lemke, A.W. McCall, S.M. Williams, J.W. Jackwood, L.A. Byrd, Virology 398, 98–108 (2010)

    Article  PubMed  CAS  Google Scholar 

  26. USDA, Title 9, Code of Federal regulations, standard requirements for IBV vaccines. Animal and Plant Health Inspection Service, US National Archives and Records Administration, College Park, MD (1999)

  27. S.A. Callison, D.A. Hilt, T.O. Boynton, B.F. Sample, R. Robison, D.E. Swayne, M.W. Jackwood, J. Virol. Methods 138, 60–65 (2006)

    Article  PubMed  CAS  Google Scholar 

  28. M.W. Jackwood, D.A. Hilt, T.P. Brown, Avian Dis. 47, 627–632 (2003)

    Article  PubMed  Google Scholar 

  29. K. Ratia, K.S. Saikatendu, B.D. Santarsiero, N. Barretto, S.C. Baker, R.C. Stevens, A.D. Mesecar, Proc. Natl. Acad. Sci. USA 103, 5717–5722 (2006)

    Article  PubMed  CAS  Google Scholar 

  30. D. Cavanagh, J.P. Picault, R. Gough, M. Hess, K. Mawditt, P. Britton, Avian Pathol. 34, 20–25 (2005)

    Article  PubMed  CAS  Google Scholar 

  31. S.G. Fang, S. Shen, F.P. Tay, D.X. Liu, Biochem. Biophys. Res. Commun. 336, 417–423 (2005)

    Article  PubMed  CAS  Google Scholar 

  32. B.W. Neuman, J.S. Joseph, K.S. Saikatendu, P. Serrano, A. Chatterjee, M.A. Johnson, L. Liao, J.P. Klaus, J.R. Yates III, K. Wuthrich, R.C. Stevens, M.J. Buchmeier, P. Kuhn, J. Virol. 82, 5279–5294 (2008)

    Article  PubMed  CAS  Google Scholar 

  33. P. Serrano, M.A. Johnson, M.S. Almeida, R. Horst, T. Herrmann, J.S. Joseph, B.W. Neuman, V. Subramanian, K.S. Saikatendu, M.J. Buchmeier, R.C. Stevens, P. Kuhn, K. Wuthrich, J. Virol. 81, 12049–12060 (2007)

    Article  PubMed  CAS  Google Scholar 

  34. T.S. Guu, L. Dong, P. Wittung-Stafshede, Y.J. Tao, Virology 379, 135–142 (2008)

    Article  PubMed  CAS  Google Scholar 

  35. Y. Piotrowski, G. Hansen, A.L. Boomaars-van der Zanden, E.J. Snijder, A.E. Gorbalenya, R. Hilgenfeld, Protein Sci. 18, 6–16 (2009)

    PubMed  CAS  Google Scholar 

  36. A. Putics, J. Slaby, W. Filipowicz, A.E. Gorbalenya, J. Ziebuhr, Adv. Exp. Med. Biol. 581, 93–96 (2006)

    Article  PubMed  CAS  Google Scholar 

  37. M. Bartlam, Y. Xu, Z. Rao, J. Struct. Funct. Genom. 8, 85–97 (2007)

    Article  CAS  Google Scholar 

  38. D. Zheng, G. Chen, B. Guo, G. Cheng, H. Tang, Cell Res. 18, 1105–1113 (2008)

    PubMed  CAS  Google Scholar 

  39. G.A. Versteeg, P.J. Bredenbeek, S.H. van den Worm, W.J. Spaan, Virology 361, 18–26 (2007)

    Article  PubMed  CAS  Google Scholar 

  40. J.R. Rodriguez-Madoz, D. Bernal-Rubio, D. Kaminski, K. Boyd, A. Fernandez-Sesma, J. Virol. 84, 4845–4850 (2010)

    Article  PubMed  CAS  Google Scholar 

  41. A. Ramachandran, C.M. Horvath, J. Interferon Cytokine Res. 29, 531–537 (2009)

    Article  PubMed  CAS  Google Scholar 

  42. H.A. Lindner, N. Fotouhi-Ardakani, V. Lytvyn, P. Lachance, T. Sulea, R. Menard, J. Virol. 79, 15199–15208 (2005)

    Article  PubMed  CAS  Google Scholar 

  43. A.E. Gorbalenya, E.V. Koonin, M.M. Lai, FEBS Lett. 288, 201–205 (1991)

    Article  PubMed  CAS  Google Scholar 

  44. P. Huang, M.M. Lai, J. Virol. 75, 5009–5017 (2001)

    Article  PubMed  CAS  Google Scholar 

  45. A.O. Pasternak, W.J. Spaan, E.J. Snijder, J. Gen. Virol. 87, 1403–1421 (2006)

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by USDA, CSREES award number 2007-35600-17786. The authors appreciate the assistance that was provided by Lauren Byrd, Carey Stewart, and Joshua Jackwood in conducting these studies.

Author information

Author notes

  1. N. D. Acevedol

    Present address: Veterinary Medical Center of Long Island, 75 Sunrise Highway, West Islip, NY, 11795, USA

  2. E. T. McKinley

    Present address: Southeast Poultry Research Laboratory, USDA, Agricultural Research Service, 934 College Station Road, Athens, GA, 30605, USA

Authors and Affiliations

  1. Department of Population Health, College of Veterinary Medicine, University of Georgia, 953 College Station Road, Athens, GA, 30602, USA

    J. E. Phillips, M. W. Jackwood, S. W. Thor, D. A. Hilt & S. M. Williams

  2. Department of Genetics, Center for Tropical and Emerging Global Diseases, University of Georgia, 500 D. W. Brooks Drive, Athens, GA, 30602, USA

    J. C. Kissinger

  3. Plant Genome Mapping Laboratory, Departments of Crop and Soil Sciences, Plant Biology, and Genetics, University of Georgia, 111 Riverbend Road, Athens, GA, 30602, USA

    A. H. Paterson, J. S. Robertson & C. Lemke

Authors
  1. J. E. Phillips
    View author publications

    Search author on:PubMed Google Scholar

  2. M. W. Jackwood
    View author publications

    Search author on:PubMed Google Scholar

  3. E. T. McKinley
    View author publications

    Search author on:PubMed Google Scholar

  4. S. W. Thor
    View author publications

    Search author on:PubMed Google Scholar

  5. D. A. Hilt
    View author publications

    Search author on:PubMed Google Scholar

  6. N. D. Acevedol
    View author publications

    Search author on:PubMed Google Scholar

  7. S. M. Williams
    View author publications

    Search author on:PubMed Google Scholar

  8. J. C. Kissinger
    View author publications

    Search author on:PubMed Google Scholar

  9. A. H. Paterson
    View author publications

    Search author on:PubMed Google Scholar

  10. J. S. Robertson
    View author publications

    Search author on:PubMed Google Scholar

  11. C. Lemke
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to M. W. Jackwood.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 46 kb)

Supplementary material 2 (DOC 37 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Phillips, J.E., Jackwood, M.W., McKinley, E.T. et al. Changes in nonstructural protein 3 are associated with attenuation in avian coronavirus infectious bronchitis virus. Virus Genes 44, 63–74 (2012). https://doi.org/10.1007/s11262-011-0668-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11262-011-0668-7

Keywords