Bovine nebovirus (BoNeV), a single-stranded positive-sense RNA virus belonging to the Caliciviridae family, genus Nebovirus, has a genome length ranging from 7453 to 7460 nt. Initially, identified in 1978 within fecal samples from calves experiencing diarrhea in the United Kingdom, BoNeV was subsequently detected in beef cattle, cows, and yaks across 13 countries spanning four continents, thereby demonstrating its extensive global distribution. Although a stable cell culture system for BoNeV is not yet available, its pathogenicity in calves has been confirmed through experimental infection studies. With the increasingly severe losses caused by viral diarrhea to calves, research on this virus has attracted widespread attention. This article reviews the latest research on the molecular epidemiology, genome structure, genetic evolution, recombination, detection methods, and pathogenesis of BoNeV. In summary, BoNeV has a high prevalence and coinfection rate, and its gene sequence is characterized by genetic diversity and a high recombination frequency. Different evolutionary subtypes of strains exhibit lower amino acid homology and structural differences. This review provides important insights for advancing future genetic evolution research and prevention strategies related to BoNeV.
| [1] |
Bridger J, Hall G, Brown J. Characterization of a calici-like virus (Newbury agent) found in association with astrovirus in bovine diarrhea. Infection and Immunity, 1984, 43: 133-138
|
| [2] |
Candido M, Alencar A, Almeida-Queiroz S, Buzinaro M, Munin F, Godoy S, Livonesi M, Fernandes A, Sousa R. First detection and molecular characterization of Nebovirus in Brazil. Epidemiology and Infection, 2016, 144: 1876-1878
|
| [3] |
Chen T, Zhu Q, Bao Z, Yu Q, Zhang J, Ren Y, Zhang Z, Zhang B. Expression of VP1 protein of bovine nebovirus by recombinant adenovirus and evaluation of its immune effect (in Chinese). Chinese Journal of Veterinary Science, 2024, 44: 268-275
|
| [4] |
Cho YI, Han J, Wang C, Cooper V, Schwartz K, Engelken T, Yoon K. Case-control study of microbiological etiology associated with calf diarrhea. Veterinary Microbiology, 2013, 166: 375-385
|
| [5] |
Cho, E. H., M. Soliman, M. Alfajaro, J. Kim, J. Seo, J. Park, D. Kim, Y. Baek, M. Kang, S. Park, K. Le Pendu, and Cho. 2018. Bovine nebovirus interacts with a wide spectrum of histo-blood group antigens. Journal of Virology 92:e02160-17. https://doi.org/10.1128/JVI.02160-17.
|
| [6] |
Deval J, Jin Z, Chuang Y, Kao C. Structure(s), function(s), and inhibition of the RNA-dependent RNA polymerase of noroviruses. Virus Research, 2017, 234: 21-33
|
| [7] |
Di Martino B, Profio Di., Martella V, Ceci C, Marsilio F. Evidence for recombination in neboviruses. Veterinary Microbiology, 2011, 153: 367-372
|
| [8] |
Eden JS, Tanaka M, Boni M, Rawlinson W, White P. Recombination within the pandemic norovirus GII.4 lineage. Journal of Virology, 2013, 87: 6270-6282
|
| [9] |
Ettayebi K, Crawford S, Murakami K, Broughman J, Karandikar U, Tenge V, Neill F, Blutt S, Zeng X, Qu L, Kou B, Opekun A, Burrin D, Graham D, Ramani S, Atmar R, Estes M. Replication of human noroviruses in stem cell-derived human enteroids. Science, 2016, 353: 1387-1393
|
| [10] |
Guo Z, He Q, Zhang B, Yue H, Tang C. First detection of neboviruses in yak (Bos grunniens) and identification of a novel neboviruses based on complete genome. Veterinary Microbiology, 2019, 236: 108388
|
| [11] |
Hall GA, Parsons K, Bridger J, Ghatei M, Ying Y, Bloom S. Plasma enteroglucagon and neurotensin levels in gnotobiotic calves infected with enteropathogenic and nonenteropathogenic viruses. Research in Veterinary Science, 1985, 38: 99-103
|
| [12] |
Hassine-Zaafrane M, Kaplon J, Sdiri-Loulizi K, Aouni Z, Pothier P, Aouni M, Ambert-Balay K. Molecular prevalence of bovine noroviruses and neboviruses detected in central-eastern Tunisia. Archives of Virology, 2012, 157: 1599-1604
|
| [13] |
Jones MK, Watanabe M, Zhu S, Graves C, Keyes L, Grau K, Gonzalez-Hernandez M, Iovine N, Wobus C, Vinje J, Tibbetts S, Wallet S, Karst S. Enteric bacteria promote human and mouse norovirus infection of B cells. Science, 2014, 346: 755-759
|
| [14] |
Kaplon J, Guenau E, Asdrubal P, Pothier P, Ambert-Balay K. Possible novel nebovirus genotype in cattle, France. Emerging Infectious Diseases, 2011, 17: 1120-1123
|
| [15] |
Le Pendu J, Abrantes J, Bertagnoli S, Guitton J, Le Gall-Reculé G, Lopes A, Marchandeau S, Alda F, Almeida T, Célio A, et al. . Proposal for a unified classification system and nomenclature of lagoviruses. Journal of General Virology, 2017, 98: 1658-1666
|
| [16] |
Li, S., 2021. Detection and molecular characteristics of bovine nebovirus in some provinces of China (in Chinese). Chengdu: Southwest Minzu University, https://doi.org/10.27417/d.cnki.gxnmc.2021.000333.
|
| [17] |
Mirabelli C, Santos-Ferreira N, Gillilland M, Cieza R, Colacino J, Sexton J, Neyts J, Taube S, Rocha-Pereira J, Wobus C. Human norovirus efficiently replicates in differentiated 3D-human intestinal enteroids. Journal of Virology, 2022, 96: e0085522
|
| [18] |
Oliver SL, Asobayire E, Dastjerdi A, Bridger J. Genomic characterization of the unclassified bovine enteric virus Newbury agent-1 (Newbury1) endorses a new genus in the family Caliciviridae. Virology, 2006, 350: 240-250
|
| [19] |
Pankovics P, Boros A, Nemes C, Delwart E, Reuter G. First detection of nebovirus (Caliciviridae) in fecal sample of diarrhoeic calf in Hungary. Magyar Allatorvosok Lapja, 2013, 135: 12-17
|
| [20] |
Park SI, Jeong C, Kim H, Park S, Park S, Hyun B, Yang D, Kim S, Kang M, Cho K. Molecular epidemiology of bovine noroviruses in South Korea. Veterinary Microbiology, 2007, 124: 125-133
|
| [21] |
Pourasgari F, Kaplon J, Sanchooli A, Fremy C, Karimi-Naghlani S, Otarod V, Ambert-Balay K, Mojgani N, Pothier P. Molecular prevalence of bovine noroviruses and neboviruses in newborn calves in Iran. Archives of Virology, 2018, 163: 1271-1277
|
| [22] |
Salim AF, Phillips A, Farthing M. Pathogenesis of gut virus infection. Baillière's Clinical Gastroenterology, 1990, 4: 593-607
|
| [23] |
Smertina E, Urakova N, Strive T, Frese M. Calicivirus RNA-dependent RNA polymerases: Evolution, structure, protein dynamics, and function. Frontiers in Microbiology, 2019, 10: 1280
|
| [24] |
Smiley JR, Chang K, Hayes J, Vinjé J, Saif L. Characterization of an enteropathogenic bovine calicivirus representing a potentially new calicivirus genus. Journal of Virology, 2002, 76: 10089-10098
|
| [25] |
Smiley JR, Hoet A, Tråvén M, Tsunemitsu H, Saif L. Reverse transcription-PCR assays for detection of bovine enteric caliciviruses (BEC) and analysis of the genetic relationships among BEC and human caliciviruses. Journal of Clinical Microbiology, 2003, 41: 3089-3099
|
| [26] |
Smith HQ, Smith T. The dynamic capsid structures of the noroviruses. Viruses, 2019, 11: 235
|
| [27] |
Sun J, Yue H, Tang C. Establishment and application of multiplex RT-PCR for detection of five bovine diarrhea viruses (in Chinese). Acta Veterinaria Et Zootechnica Sinica, 2022, 53: 209-218
|
| [28] |
Thomas C, Jung K, Han M, Hoet A, Scheuer K, Wang Q, Saif L. Retrospective serosurveillance of bovine norovirus (GIII.2) and nebovirus in cattle from selected feedlots and a veal calf farm in 1999 to 2001 in the United States. Archives of Virology, 2014, 159: 83-90
|
| [29] |
Turan T, Işıdan H, Atasoy M, Irehan B. Detection and molecular analysis of bovine enteric norovirus and nebovirus in Turkey. Journal of Veterinary Research, 2018, 62: 129-135
|
| [30] |
Wang HM. Isolation and genome sequence of murine norovirus strain SH1603 in China and identification the human norovirus infectious clone (in Chinese), 2017, Hohhot. Inner Mongolia Medical University
|
| [31] |
Wang, Z., 2021. Establishment and application of two indirect ELISA methods based on prokaryotic expression of recombinant protein of bovine nebovirus and bovine norovirus VP1 (in Chinese). Chengdu: Southwest Minzu University. https://doi.org/10.27417/d.cnki.gxnmc.2021.000251.
|
| [32] |
Woode GN, Bridger J. Isolation of small viruses resembling astroviruses and caliciviruses from acute enteritis of calves. Journal of Medical Microbiology, 1978, 11: 441-452
|
| [33] |
Yilmaz A, Bostan K, Altan E, Muratoglu K, Turan N, Tan D, Helps C, Yilmaz H. Investigations on the frequency of norovirus contamination of ready-to-eat food items in Istanbul, Turkey, by using real-time reverse transcription PCR. Journal of Food Protection, 2011, 74: 840-843
|
| [34] |
Zhao R, Wang X, Hou L, Zhang H, Zhao Y, Zhang Z, Zhou W. Establishment and application of TaqMan real-time quantitative RT-PCR method for the detection of bovine nebovirus (in Chinese). Chinese Journal of Veterinary Medicine, 2023, 43: 66-71
|
| [35] |
Zhou J, Li C, Liu X, Chiu M, Zhao X, Wang D, Wei Y, Lee A, Zhang A, Chu H, et al. . Infection of bat and human intestinal organoids by SARS-CoV-2. Nature Medicine, 2020, 26: 1077-1083
|
| [36] |
Zhu Q, Li B, Sun D. Advances in bovine coronavirus epidemiology. Viruses, 2022, 14: 1109
|
| [37] |
Zhu Q, Li B, Sun D. Bovine astrovirus-a comprehensive review. Viruses, 2022, 14: 1217
|
| [38] |
Zhu Q, Su M, Li Z, Wang X, Qi S, Zhao F, Li L, Guo D, Feng L, Li B, Sun D. Epidemiological survey and genetic diversity of bovine coronavirus in Northeast China. Virus Research, 2022, 308: 198632
|
| [39] |
Zhu Q, Qi S, Guo D, Li C, Su M, Wang J, Li Z, Yang D, Sun H, Wang X, et al. . A survey of fecal virome and bacterial community of the diarrhea-affected cattle in northeast China reveals novel disease-associated ecological risk factors. mSystems, 2024, 9: e0084223
|
Funding
Introducing Talents Scientific Research Start-up Project of Heilongjiang Bayi Agricultural University(XYB202510)
The Project funding for excellent master's and doctoral theses in Longjiang in the new era(LJYXL2023-100)
The Key Project of Natural Science Foundation of Heilongjiang Province of China (ZD2023C006)
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The Author(s)