Skip to main content
SpringerLink
Log in

Detection and genetic analysis of bovine rhinitis B virus in Japan

  • Original Article
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

Bovine rhinitis B virus (BRBV) (genus Aphthovirus, family Picornaviridae) is a significant etiological agent of the bovine respiratory disease complex. Despite global reports on BRBV, genomic data for Japanese strains are not available. In this study, we aimed to obtain genomic information on BRBV in Japan and analyze its genetic characteristics. In nasal swabs from 66 cattle, BRBV was detected in 6 out of 10 symptomatic and 4 out of 56 asymptomatic cattle. Using metagenomic sequencing and Sanger sequencing, the nearly complete genome sequences of two Japanese BRBV strains, IBA/2211/2 and LAV/238002, from symptomatic and asymptomatic cattle, respectively, were determined. These viruses shared significant genetic similarity with known BRBV strains and exhibited unique mutations and recombination events, indicating dynamic evolution, influenced by regional environmental and biological factors. Notably, the leader gene was only approximately 80% and 90% identical in its nucleotide and amino acid sequence, respectively, to all of the BRBV strains with sequences in the GenBank database, indicating significant genetic divergence in the Japanese BRBV leader gene. These findings provide insights into the genetic makeup of Japanese BRBV strains, enriching our understanding of their genetic diversity and evolutionary mechanisms.

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

Access this article

Log in via an institution

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

Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  1. Zell R, Delwart E, Gorbalenya AE, Hovi T, King AMQ, Knowles NJ, Lindberg AM, Pallansch MA, Palmenberg AC, Reuter G, Simmonds P, Skern T, Stanway G, Yamashita T, Ictv Report Consortium (2017) ICTV virus taxonomy profile: picornaviridae. J Gen Virol 98:2421–2422. https://doi.org/10.1099/jgv.0.000911

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Hollister JR, Vagnozzi A, Knowles NJ, Rieder E (2008) Molecular and phylogenetic analyses of bovine rhinovirus type 2 shows it is closely related to foot-and-mouth disease virus. Virology 373:411–425. https://doi.org/10.1016/j.virol.2007.12.019

    Article  CAS  PubMed  Google Scholar 

  3. Reed SE, Tyrrell DA, Betts AO, Watt RG (1971) Studies on a rhinovirus (EC11) derived from a calf. I. Isolation in calf tracheal organ cultures and characterization of the virus. J Comp Pathol 81:33–40. https://doi.org/10.1016/0021-997590052-1

    Article  CAS  PubMed  Google Scholar 

  4. Mitra N, Cernicchiaro N, Torres S, Li F, Hause BM (2016) Metagenomic characterization of the virome associated with bovine respiratory disease in feedlot cattle identified novel viruses and suggests an etiologic role for influenza D virus. J Gen Virol 97:1771–1784. https://doi.org/10.1099/jgv.0.000492

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Ng TF, Kondov NO, Deng X, Van Eenennaam A, Neibergs HL, Delwart E (2015) A metagenomics and case-control study to identify viruses associated with bovine respiratory disease. J Virol 89:5340–5349. https://doi.org/10.1128/JVI.00064-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Zhang M, Hill JE, Fernando C, Alexander TW, Timsit E, van der Meer F, Huang Y (2019) Respiratory viruses identified in western Canadian beef cattle by metagenomic sequencing and their association with bovine respiratory disease. Transbound Emerg Dis 66:1379–1386. https://doi.org/10.1111/tbed.13172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Bhattarai S, Lin CM, Temeeyasen G, Palinski R, Li F, Kaushik RS, Hause BM (2022) Bovine rhinitis B virus is highly prevalent in acute bovine respiratory disease and causes upper respiratory tract infection in calves. J Gen Virol 103:001714. https://doi.org/10.1099/jgv.0.001714

    Article  PubMed  PubMed Central  Google Scholar 

  8. Hause BM, Collin EA, Anderson J, Hesse RA, Anderson G (2015) Bovine rhinitis viruses are common in U.S. cattle with bovine respiratory disease. PLOS One 10:e0121998. https://doi.org/10.1371/journal.pone.0121998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Tosh C, Hemadri D, Sanyal A (2002) Evidence of recombination in the capsid-coding region of type A foot-and-mouth disease virus. J Gen Virol 83:2455–2460. https://doi.org/10.1099/0022-1317-83-10-2455

    Article  CAS  PubMed  Google Scholar 

  10. Rai DK, Lawrence P, Pauszek SJ, Piccone ME, Knowles NJ, Rieder E (2016) Bioinformatics and molecular analysis of the evolutionary relationship between bovine rhinitis A viruses and foot-and-mouth disease virus. Bioinform Biol Insights 4:43–58. https://doi.org/10.4137/BBI.S37223

    Article  Google Scholar 

  11. Zhou Y, Chen X, Tang C, Yue H (2023) Detection and genomic characterization of bovine rhinitis virus in China. Animals 13:312. https://doi.org/10.3390/ani13020312

    Article  PubMed  PubMed Central  Google Scholar 

  12. Kishimoto M, Tsuchiaka S, Rahpaya SS, Hasebe A, Otsu K, Sugimura S, Kobayashi S, Komatsu N, Nagai M, Omatsu T, Naoi Y, Sano K, Okazaki-Terashima S, Oba M, Katayama Y, Sato R, Asai T, Mizutani T (2017) Development of a one-run real-time PCR detection system for pathogens associated with bovine respiratory disease complex. J Vet Med Sci 79:517–523. https://doi.org/10.1292/jvms.16-0489

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882. https://doi.org/10.1093/nar/25.24.4876

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Tamura K, Stecher G, Kumar S (2021) MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol 38:3022–3027. https://doi.org/10.1093/molbev/msab120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  PubMed  Google Scholar 

  16. Martin DP, Murrell B, Golden M, Khoosal A, Muhire B (2015) RDP4: detection and analysis of recombination patterns in virus genomes. Virus Evol 1:vev003. https://doi.org/10.1093/ve/vev003

    Article  PubMed  PubMed Central  Google Scholar 

  17. Lole KS, Bollinger RC, Paranjape RS, Gadkari D, Kulkarni SS, Novak NG, Ingersoll R, Sheppard HW, Ray SC (1999) Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. J Virol 73:152–160. https://doi.org/10.1128/JVI.73.1.152-160.1999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Holman DB, Timsit E, Alexander TW (2015) The nasopharyngeal microbiota of feedlot cattle. Sci Rep 5:15557. https://doi.org/10.1038/srep1555

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Holman DB, Timsit E, Amat S, Abbott DW, Buret AG, Alexander TW (2017) The nasopharyngeal microbiota of beef cattle before and after transport to a feedlot. BMC Microbiol 17:70. https://doi.org/10.1186/s12866-017-0978-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Ashkani J, Rees DJ (2016) The critical role of VP1 in forming the necessary cavities for receptor-mediated entry of FMDV to the host cell. Sci Rep 6:27140. https://doi.org/10.1038/srep27140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Mason PW, Grubman MJ, Baxt B (2003) Molecular basis of pathogenesis of FMDV. Virus Res 91:9–32. https://doi.org/10.1016/s0168-1702(02)00257-5

    Article  CAS  PubMed  Google Scholar 

  22. Sherry B, Rueckert R (1985) Evidence for at least two dominant neutralization antigens on human rhinovirus 14. J Virol 53:137–143. https://doi.org/10.1128/JVI.53.1.137-143.1985

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Sherry B, Mosser AG, Colonno RJ, Rueckert RR (1986) Use of monoclonal antibodies to identify four neutralization immunogens on a common cold picornavirus, human rhinovirus 14. J Virol 57:246–257. https://doi.org/10.1128/JVI.57.1.246-257.1986

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. King DJ, Freimanis G, Neil C, Shaw A, Tuthill TJ, Laing E, King DP, Lasecka-Dykes L (2022) Establishing an in vitro system to assess how specific antibodies drive the evolution of foot-and-mouth disease virus. Viruses 14:1820. https://doi.org/10.3390/v14081820

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Ao D, Guo HC, Sun SQ, Sun DH, Fung TS, Wei YQ, Han SC, Yao XP, Cao SZ, Liu DX, Liu XT (2015) Viroporin activity of the foot-and-mouth disease virus non-structural 2B protein. PLoS One 10:e0125828. https://doi.org/10.1371/journal.pone.0125828

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Moffat K, Knox C, Howell G, Clark SJ, Yang H, Belsham GJ, Ryan M, Wileman T (2007) Inhibition of the secretory pathway by foot-and-mouth disease virus 2BC protein is reproduced by coexpression of 2B with 2C, and the site of inhibition is determined by the subcellular location of 2C. J Virol 81:1129–1139. https://doi.org/10.1128/JVI.00393-06

    Article  CAS  PubMed  Google Scholar 

  27. Ambrose RK, Blakebrough-Hall C, Gravel JL, Gonzalez LA, Mahony TJ (2013) Characterisation of the upper respiratory tract virome of feedlot cattle and its association with bovine respiratory disease. Viruses 15:455. https://doi.org/10.3390/v15020455

    Article  CAS  Google Scholar 

  28. Yang X, Hu Z, Zhang Q, Fan S, Zhong Y, Guo D, Qin Y, Chen M (2019) SG formation relies on eIF4GI-G3BP interaction which is targeted by picornavirus stress antagonists. Cell Discov 5:1. https://doi.org/10.1038/s41421-018-0068-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Grubman MJ, Baxt B (2004) Foot-and-mouth disease. Clin Microbiol Rev 17:465–493. https://doi.org/10.1128/cmr.17.2.465-493.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Belsham GJ, Brangwyn JK (1990) A region of the 5′ noncoding region of foot-and-mouth disease virus RNA directs efficient internal initiation of protein synthesis within cells: involvement with the role of L protease in translational control. J Virol 64:5389–5395. https://doi.org/10.1128/JVI.64.11.5389-5395.1990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Moral-Lopez P, Alvarez E, Redondo N, Skern T, Carrasco L (2014) L protease from foot and mouth disease virus confers eIF2-independent translation for mRNAs bearing picornavirus IRES. FEBS Lett 588:4053–4059. https://doi.org/10.1016/j.febslet.2014.09.030

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge the grants received from the Japan Society for the Promotion of Science for this research. We would like to thank Enago for their assistance in improving the English language quality of our manuscript.

Funding

This work was supported by grants-in-aid from the Japan Society for the Promotion of Science (grant numbers 22K20619 and 23K14097).

Author information

Authors and Affiliations

  1. School of Veterinary Medicine, Azabu University, Sagamihara, Kanagawa, Japan

    Hiroho Ishida, Mikari Nakamura, Hironobu Murakami, Kei Kazama, Mami Oba & Makoto Nagai

  2. Center for Infectious Disease Epidemiology and Prevention Research, Tokyo University of Agriculture and Technology, Fuchu, Tokyo, Japan

    Mami Oba, Hitoshi Takemae & Tetsuya Mizutani

  3. Beef Cattle Institute, Ibaraki Prefecture of Livestock Research Center, Hitachi-Omiya, Ibaraki, Japan

    Yoshinao Ouchi

  4. Ibaraki Prefecture Kennan Livestock Hygiene Service Center, Tsuchiura, Ibaraki, Japan

    Junko Kawakami & Satoko Tsuzuku

Authors
  1. Hiroho Ishida
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mikari Nakamura
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hironobu Murakami
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kei Kazama
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mami Oba
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hitoshi Takemae
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Tetsuya Mizutani
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yoshinao Ouchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Junko Kawakami
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Satoko Tsuzuku
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Makoto Nagai
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Hiroho Ishida: conceptualization, investigation, formal analysis, funding acquisition, writing—original draft. Mikari Nakamura: investigation, validation, visualization. Hironobu Murakami: formal analysis, writing—review & editing. Kei Kazama: resources, investigation. Mami Oba: data curation. Hitoshi Takemae: data curation. Tetsuya Mizutani: methodology, supervision. Yoshinao Ouchi: resources. Junko Kawakami: resources. Satoko Tsuzuku: resources. Makoto Nagai: writing—review & editing, supervision.

Corresponding author

Correspondence to Hiroho Ishida.

Ethics declarations

Ethical approval

The swab samples that were used in this study were collected for pathological testing of cattle; therefore, no specific approval was needed.

Conflict of interest

The authors have no relevant financial or non-financial interests to disclose.

Additional information

Handling Editor: Pablo Pineyro

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 182 KB)

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

Ishida, H., Nakamura, M., Murakami, H. et al. Detection and genetic analysis of bovine rhinitis B virus in Japan. Arch Virol 169, 125 (2024). https://doi.org/10.1007/s00705-024-06046-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00705-024-06046-y

Search

Navigation