SpringerLink
Log in

Molecular characterization of G and F protein genes of bovine respiratory syncytial virus detected from dead calves caused by severe respiratory syndrome: emergence of novel mutations and their importance

  • Original Article
  • Published:
VirusDisease Aims and scope Submit manuscript

Abstract

Bovine respiratory syncytial virus (BRSV) is an important viral agent in bovine respiratory disease complex affecting young calves from asymptomatic to fatal. Although BRSV is widely prevalent in Türkiye as in other parts of the world, there are limited molecular studies on BRSV in Türkiye. Therefore, in order to better understand the characteristics of circulating BRSV in Türkiye, a study based on the molecular analysis of both F and G proteins was performed. For this purpose, the presence of BRSV was investigated in 20 calves that died as a result of severe respiratory syndrome in the western region of Türkiye in 2020. Nested PCR was performed for both gene regions, and the products were sequenced. Four samples detected as BRSV positive were identified as genotype III according to both gene regions in molecular analysis. However, they were separated into two distinct clusters due to significant differences in nucleotide (90.09–99.54%) and amino acid (85.42–99.31%) similarities between them. Besides, two positive samples in the same cluster were even more different from previously detected Turkish isolates (90.78–92.17% nt and 87.50–89.58% aa). More over, we detected nine novel aa mutations in the extracellular domain, an immunologically important region in the G protein of the virus, that have not been reported in other world isolates found in Genbank until now. These findings suggest that there may be many different viruses in circulation that have the ability to escape the immune system. We recommend that these findings be taken into account in planning both vaccine and epidemiological studies.

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+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Canada)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Data availability

All data generated or analysed during this study are included in this published article. The datasets generated for this study can be found in NCBI, MW892048, MW892049, MW892050 and MZ476914 for F gene; MW892044, MW892045, MW892046 and MW892047 for G gene of the detected BRSV.

References

  1. Alkan F, Ozkul A, Bilge Dagalp S, Yesilbag K, Oguzoglu TC, Akça Y, Burgu I. Virological and serological studies on the role of PI-3 virus, BRSV, BVDV and BHV-1 on respiratory infections of cattle I The detection of etiological agents by direct immunofluorescence technique. Dtsch Tierarztl Wochenschr. 2000;107(5):193–5.

    CAS  PubMed  Google Scholar 

  2. Alkan F, Özkul A, Karaoglu MT, Bilge S, Akça Y, Burgu I, Yesilbag K, Oğuzoğlu TC. Sığırlarda viral nedenli solunum sistemi enfeksiyonlarinin seroepidemiyolojisi. Ankara Üniv Vet Fak Derg. 1997;44:73–80. https://doi.org/10.1501/Vetfak_0000000658.

    Article  Google Scholar 

  3. Alpay G, Tuncer P, Yeşilbağ K. Bir ada ekosistemindeki sığır, koyun ve keçilerde bazı viral enfeksiyonların serolojik olarak araştırılması. Ankara Üniv Vet Fak Derg. 2014;61:43–8. https://doi.org/10.1501/Vetfak_0000002603.

    Article  Google Scholar 

  4. Avci O, Yavru S, Ekik M. Detection of respiratory viral antigens in cattle lung tissues by direct ELISA. Anim Vet Sci. 2014;2:146–9.

    Article  Google Scholar 

  5. Avci O, Yavru S, Sevik M. Antibody prevalence against respiratory viruses in naturally infected cattle in Central Anatolia. Eurasian J Vet Sci. 2014;30(2):80–4.

    Google Scholar 

  6. Baptista AL, Rezende AL, Fonseca PDA, Massi RP, Nogueira GM, Magalhães LQ, Headley SA, Menezes GL, Alfieri AA, Saut JPE. Bovine respiratory disease complex associated mortality and morbidity rates in feedlot cattle from southeastern Brazil. J Infect Dev Ctries. 2017;11:791–9. https://doi.org/10.3855/jidc.9296.

    Article  PubMed  Google Scholar 

  7. Bertolotti L, Giammarioli M, Rosati S. Genetic characterization of bovine respiratory syncytial virus strains isolated in Italy: evidence for the circulation of new divergent clades. J Vet Diagn Investig. 2018;30:300–4. https://doi.org/10.1177/1040638717746202.

    Article  Google Scholar 

  8. Beuttemmuller EA, Alfieri AF, Headley SA, Alfieri AA. Brazilian strain of bovine respiratory coronavirus is derived from dual enteric and respiratory tropism. Genet Mol Res. 2017;16(2):gmr16029580. https://doi.org/10.4238/gmr16029580.

    Article  Google Scholar 

  9. Burgu I, Toker A, Akca Y, Alkan F. Seroepidemiologic study of bovine respiratory syncytial virus (BRSV) in Turkey. Dtsch Tierarztl Wochenschr. 1990;97(2):88–9.

    CAS  PubMed  Google Scholar 

  10. Çabalar M, Can Şahna K. Doğu ve güneydoğu anadolu bölgesinde süt sığırlarında parainfluenza virus-3, bovine herpes virus-1 ve respiratory syncytial virus enfeksiyonlarının seroepidemiyolojisi. YYÜ Vet Fak Derg. 2000;11:101–5.

    Google Scholar 

  11. Chang Y, Yue H, Tang C. Prevalence and molecular characteristics of bovine respiratory syncytial virus in beef cattle in China. Animals. 2022;12:3511. https://doi.org/10.3390/ani12243511.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Duman R, Yavru S, Kale M, Avcı O. Seroprevalence of viral upper respiratory infections in dairy cattle. Kafkas Univ Vet Fak Derg. 2009;15(4):539–42.

    Google Scholar 

  13. Fulton RW. Bovine respiratory disease research (1983–2009). Anim Health Res Rev. 2009;10:131–9. https://doi.org/10.1017/S146625230999017X.

    Article  PubMed  Google Scholar 

  14. Furze J, Roberts SR, Wertz G, Taylor G. Antigenically distinct G glycoproteins of BRSV strains share a high degree of genetic homogeneity. Virology. 1997;231:48–58. https://doi.org/10.1006/viro.1997.8490.

    Article  CAS  PubMed  Google Scholar 

  15. Furze J, Wertz G, Lerch Taylor G. Antigenic heterogenicity of the attachment protein of bovine respiratory syncytial virus. J Gen Virol. 1994;75:363–70. https://doi.org/10.1099/0022-1317-75-2-363.

    Article  CAS  PubMed  Google Scholar 

  16. Gershwin LJ, Van Eenennaam AL, Tisioto PC, Kim J, Seabury CM, Taylor JF, Neibergs H L. The host gene expression response to specific BRD pathogens. In: American Association of bovine practitioners conference proceedings; 2015. p. 157–60.

  17. Hall T. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser. 1999;41:95–8.

    CAS  Google Scholar 

  18. Headley SA, Okano W, Balbo LC, Marcasso RA, Oliveira TE, Alfieri AF, NegriFilho LC, Michelazzo MZ, Rodrigues SC, Baptista AL, Saut SJP, Alfieri AA. Molecular survey of infectious agents associated with bovine respiratory disease in a beef cattle feedlot in southern Brazil. J Vet Diagn Invest. 2018;30:249–51. https://doi.org/10.1177/1040638717739945.

    Article  PubMed  Google Scholar 

  19. International Committee on Taxonomy of Viruses. 2019. https://talk.ictvonline.org/ictv-reports/ictv_online_report/negative-sense-rnaviruses/mononegavirales/w/pneumoviridae/738/genus-orthopneumovirus. Accessed March 2022.

  20. Ince OM, Sevik M, Ozgur EG, Sait A. Risk factors and genetic characterization of bovine respiratory syncytial virus in the inner Aegean Region, Turkey. Trop Anim Health Prod. 2022;54(1):4. https://doi.org/10.1007/s11250-021-03022-5.

    Article  Google Scholar 

  21. Karayel Hacioglu I, Coskun N, Duran Yelken S, Sevinc S, Alkan F. Phylogenetic analysis of bovine respiratory syncytial virus form calves with respiratory disorders. Kafkas Univ Vet Fak Derg. 2019;25(2):251–9. https://doi.org/10.9775/kvfd.2018.20819.

    Article  Google Scholar 

  22. Klem TB, Kjæstad HP, Kummen E, Holen H, Stokstad M. Bovine respiratory syncytial virus outbreak reduced bulls’ weight gain and feed conversion for eight months in a Norwegian beef herd. Acta Vet Scand. 2016;58:8. https://doi.org/10.1186/s13028-016-0190-y.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Klem TB, Rimstad E, Stokstad M. Occurrence and phylogenetic analysis of bovine respiratory syncytial virus in outbreaks of respiratory disease in Norway. BMC Vet Res. 2014;10:1–9. https://doi.org/10.1186/1746-6148-10-15.

    Article  Google Scholar 

  24. Kresic N, Bedekovic T, Brnic D, Simic I, Lojkic I, Turk N. Genetic analysis of bovine respiratory syncytial virus in Croatia. Comp Immunol Microbiol Infect Dis. 2018;58:52–7. https://doi.org/10.1016/j.cimid.2018.09.004.

    Article  PubMed  Google Scholar 

  25. Kumagai A, Kawauchi K, Andoh K, Hatama S. Sequence and unique phylogeny of G genes of bovine respiratory syncytial viruses circulating in Japan. J Vet Diagn Investig. 2021;33(1):162–6. https://doi.org/10.1177/1040638720975364.

    Article  CAS  Google Scholar 

  26. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35(6):1547–9. https://doi.org/10.1093/molbev/msy096.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Langedijk JP, Meloen RH, Taylor G, Furze JM, van Oirschot JT. Antigenic structure of the central conserved region of protein G of bovine respiratory syncytial virus. J Virol. 1997;71:4055–61. https://doi.org/10.1128/jvi.71.5.4055-4061.1997.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Larsen LE, Tjørnehøj K, Viuff B. Extensive sequence divergence among bovine respiratory syncytial viruses isolated during recurrent outbreaks in closed herds. J Clin Microbiol. 2000;38:4222–7. https://doi.org/10.1128/JCM.38.11.4222-4227.2000.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Leme RA, Agnol AMD, Balbo LC, Pereria FL, Possatti F, Alfieri AF, Alfieri AA. Molecular characterization of Brazilian wild-type strains of Bovine respiratory syncytial virus reveals genetic diversity and putative subgroup of the virus. Vet Q. 2020;40:83–96. https://doi.org/10.1080/01652176.2020.1733704.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Lerch RA, Anderson K, Wertz GW. Nucleotide suquence analysis and expression from recombinant vectors demonstrate that the attachment protein G of bovine respiratory syncytial virus is distinct from that of human respiratory syncytial virus. J Virol. 1990;64:5559–69. https://doi.org/10.1128/jvi.64.11.5559-5569.1990.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Neill JD, Ridpath JF, Valayudhan BT. Identification and genome characterization of genotype B and genotype C of bovine parainfluenza type 3 viruses isolated in the United States. BMC Vet Res. 2015;11:112. https://doi.org/10.1186/s12917-015-0431-8.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Prozzi D, Walravens K, Langedijk JPM, Daus F, Kramps JA, Letesson JJ. Antigenic and molecular analyses of the variability of bovine respiratory syncytial virus G glycoprotein. J Gen Virol. 1997;78(2):359–66. https://doi.org/10.1099/0022-1317-78-2-359.

    Article  CAS  PubMed  Google Scholar 

  33. Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19(12):1572–4. https://doi.org/10.1093/bioinformatics/btg180.

    Article  CAS  PubMed  Google Scholar 

  34. Sarmiento-Silva RE, Nakamura-Lopez Y, Vaughan G. Epidemiology, molecular epidemiology, and evolution of bovine respiratory syncytial virus. Viruses. 2012;4:3452–67. https://doi.org/10.3390/v4123452.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Schrijver RS, Daus F, Kramps JA, Langedijk JPM, Buijs R, Middel WGJ, Taylor G, Furze J, Huyben MWC, van Oirschot JT. Subgrou** of bovine respiratory syncytial virus strains detected in lung tissue. Vet Microbiol. 1996;53(3–4):253–60. https://doi.org/10.1016/S0378-1135(96)01223-0.

    Article  CAS  PubMed  Google Scholar 

  36. Socha W, Larska M, Rola J. Molecular characterisation of the first polish isolates of bovine respiratory syncytial virus. Bull Vet Inst Pulawy. 2009;53:569–74.

    Google Scholar 

  37. Taylor G, Thomas LH, Furze JM, Cook RS, Wyld SG, Lerch R, Hardy R, Wertz GW. Recombinant vaccinia viruses expressing the F, G or N, but not the M2, protein of bovine respiratory syncytial virus (BRSV) induce resistance to BRSV challenge in the calf and protect aganist the development of pneumonic lesions. J Gen Virol. 1997;44:191–5. https://doi.org/10.1099/0022-1317-78-12-3195.

    Article  Google Scholar 

  38. Taylor G, Wyld S, Valarcher JF, Guzman E, Thom M, Widdison S, Buchholz UJ. Recombinant bovine respiratory syncytial virus with deletion of the SH gene induces increased apoptosis and pro-inflammatory cytokines in vitro, and is attenuated and induces protective immunity in calves. J Gen Virol. 2014;95:1244–54. https://doi.org/10.1099/vir.0.064931-0.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Thonur L, Maley M, Gilray J, Crook T, Laming E, Turnbull D, Nath M, Willoughby K. One-step multiplex real time RT-PCR for the detection of bovine respiratory syncytial virus, bovine herpesvirus 1 and bovine parainfluenza virus 3. BMC Vet Res. 2012;8:37. https://doi.org/10.1186/1746-6148-8-37.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Timurkan MO, Aydin H, Sait A. Identification and molecular characterisation of bovine parainfluenza virus-3 and bovine respiratory syncytial virus-first report form Turkey. J Vet Res. 2019;63:167–73. https://doi.org/10.2478/jvetres-2019-0022.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Toker EB, Yeşilbağ K. Molecular characterization and comprarison of diagnostic methods for bovine respiratory viruses (BPIV-3, BRSV, BVDV, and BoHV-1) in field samples in Northwestern Turkey. Trop Anim Health Prod. 2021;53:79. https://doi.org/10.1007/s11250-020-02489-y.

    Article  PubMed  Google Scholar 

  42. Urban-Chmiel R, Wernicki A, Puchalski A, Dec M, Stęgierska D, Grooms DL, Barbu NI. Detection of bovine respiratory syncytial virus infections in young dairy and beef cattle in Poland. Vet Q. 2014;35:33–6. https://doi.org/10.1080/01652176.2014.984366.

    Article  PubMed  Google Scholar 

  43. Valarcher JF, Schelcher F, Bourhy H. Evolution of bovine respiratory syncytial virus. J Virol. 2000;74:10714–28. https://doi.org/10.1128/JVI.74.22.1071410728.2000.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Valarcher JF, Taylor G. Bovine respiratory syncytial virus infection. Vet Res. 2007;38(2):153–80. https://doi.org/10.1051/vetres:2006053.

    Article  CAS  PubMed  Google Scholar 

  45. Valentova V. The antigenic and genetic variability of bovine respiratory syncytial virus with emphasis on the G protein. Vet Med. 2003;48:254–66. https://doi.org/10.17221/5778-VETMED.

    Article  CAS  Google Scholar 

  46. Valentova V, Antonis AFG, Kovarcik K. Restriction enzyme analysis of RT-PCR amplicons as a rapid method for detection of genetic diversity among bovine respiratory syncytial virus isolates. Vet Microbiol. 2005;108:1–12. https://doi.org/10.1016/j.vetmic.2005.02.008.

    Article  CAS  PubMed  Google Scholar 

  47. Yavru S, Şimşek A, Yapkıç O, Kale M. Serological evaluation of viral infections in bovine respiratory tract. Acta Vet-Beograd. 2005;55:219–26. https://doi.org/10.2298/AVB0503219Y.

    Article  Google Scholar 

  48. Yazici Z, Ozan E, Tamer C, Muftuoglu B, Barry G, Kurucay HN, Elhag AE, Cagirgan AA, Gumusova S, Albayrak H. Circulation of indigenous bovine respiratory syncytial virus strains in Turkish Cattle: the first isolation and molecular characterization. Animals. 2020;10:1700. https://doi.org/10.3390/ani10091700.

    Article  PubMed  PubMed Central  Google Scholar 

  49. Yeşilbağ K, Güngör B. Seroprevalence of bovine respiratory viruses in North-Western Turkey. Trop Anim Health Prod. 2008;40(1):55–60. https://doi.org/10.1007/s11250-007-9053-x.

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This study was supported and officially permissied by Ministry of Agriculture and Forestry of The Republic of Türkiye.

Funding

This study was supported and funded by Agriculture and Foresty of the Republic of Türkiye and İzmir/Bornova Veterinary Control Institute.

Author information

Authors and Affiliations

  1. Virology Department, Izmir/Bornova Veterinary Control Institute, 35040, Izmir, Turkey

    Murat Kaplan, Kemal Pekmez, Abdurrahman Anıl Çağırgan & Fatih Arslan

  2. Department of Veterinary Experimental Animals, Faculty of Veterinary Medicine, Ondokuz Mayis University, 55139, Samsun, Turkey

    Emre Özan

Authors
  1. Murat Kaplan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Emre Özan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kemal Pekmez
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Abdurrahman Anıl Çağırgan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Fatih Arslan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Murat Kaplan or Emre Özan.

Ethics declarations

Conflicts of interest

The authors declare that they have no conflict of interest.

Consent for publication

The manuscript was approved and permissioned as officialy by Ministry of Agriculture and Forestry.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kaplan, M., Özan, E., Pekmez, K. et al. Molecular characterization of G and F protein genes of bovine respiratory syncytial virus detected from dead calves caused by severe respiratory syndrome: emergence of novel mutations and their importance. VirusDis. 34, 539–549 (2023). https://doi.org/10.1007/s13337-023-00846-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13337-023-00846-7

Keywords

Search

Navigation