Summary.
Bovine enteric noroviruses form a genogroup, III, distinct from the 2 human norovirus genogroups, I and II. Two genogroup III genotypes were suggested by partial genomic analyses. In the present study, analysis of the full-length genome sequence of Bo/Newbury2/76/UK and the more contemporary Newbury2-like virus, Bo/Dumfries/1994/UK, showed that both were 7311 nucleotides in length and had three open reading frames (ORFs), amino acids motifs typical of noroviruses, and 95% or greater amino acid identities to each other in all regions of their genome. Apart from the ORF1 NTPase region, their ORF1 regions had less than 90% identity to the genogroup III genotype 1 Bo/Jena/80/DE virus, confirming two genogroup III genotypes. A close antigenic relationship was demonstrated by ELISA between the genotype 2 viruses, which will allow their serological diagnosis.
Keywords: ORF1 Gene, Calf Diarrhoea, Human Noroviruses, Complete Genomic Characterization, Bovine Noroviruses
Footnotes
Deceased [Fourth Author]
References
- Ando T, Noel JS, Fankhauser RL. Genetic classification of “Norwalk-like viruses”. J Infect Dis. 2000;181:S336–S348. doi: 10.1086/315589. [DOI] [PubMed] [Google Scholar]
- Andrews AH. Calf enteritis – New information from NADIS. UK VET. 2000;5:30–34. [Google Scholar]
- Bridger JC, Hall GA, Brown JF. Characterization of a calici-like virus (Newbury agent) found in association with astrovirus in bovine diarrhoea. Infect Immunol. 1984;43:133–138. doi: 10.1128/iai.43.1.133-138.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Clarke IN, Lambden PR. Organization and expression of calicivirus genes. J Infect Dis. 2000;181:S309–S316. doi: 10.1086/315575. [DOI] [PubMed] [Google Scholar]
- Dastjerdi AM, Green J, Gallimore CI, Brown DW, Bridger JC. The bovine Newbury agent-2 is genetically more closely related to human SRSVs than to animal caliciviruses. Virology. 1999;254:1–5. doi: 10.1006/viro.1998.9514. [DOI] [PubMed] [Google Scholar]
- Deng Y, Batten CA, Liu BL, Lambden PR, Elschner M, Gunther H, Otto P, Schnurch P, Eichhorn W, Herbst W, Clarke IN. Studies of epidemiology and seroprevalence of bovine noroviruses in Germany. J Clin Microbiol. 2003;41:2300–2305. doi: 10.1128/JCM.41.6.2300-2305.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dingle KE, Lambden PR, Caul EO, Clarke IN. Human enteric Caliciviridae: the complete genome sequence and expression of virus-like particles from a genetic group II small round structured virus. J Gen Virol. 1995;76:2349–2355. doi: 10.1099/0022-1317-76-9-2349. [DOI] [PubMed] [Google Scholar]
- Glass PJ, White LJ, Ball JM, Leparc-Goffart I, Hardy ME, Estes MK. Norwalk virus open reading frame 3 encodes a minor structural protein. J Virol. 2000;74:6581–6591. doi: 10.1128/JVI.74.14.6581-6591.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gray JJ, Cunliffe C, Ball J, Graham DY, Desselberge U, Estes MK. Detection of immunoglobulin M (IgM), IgA, and IgG Norwalk virus-specific antibodies by indirect enzyme-linked immunosorbent assay with baculovirus-expressed Norwalk virus capsid antigen in adult volunteers challenged with Norwalk virus. J Clin Microbiol. 1994;32:3059–3063. doi: 10.1128/jcm.32.12.3059-3063.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Green KY, Chanock RM, Kapikian AZ. Human caliciviruses. In: Griffin DE, Lamb RA, Martin MA, Roizman B, Straws SE, editors. Fields virology. Philadelphia: Lippincott, Williams and Wilkins; 2001. pp. 841–874. [Google Scholar]
- Gunther H, Otto P. Diarrhoea in young calves. 7. Zackenvirus (Jena agent 117/80) – a new diarrhoea pathogen in calves. Arch Exp Veterinarmed. 1987;41:934–938. [PubMed] [Google Scholar]
- Hale AD, Crawford SE, Ciarlet M, Green J, Gallimore C, Brown DW, Jiang X, Estes MK. Expression and self-assembly of Grimsby virus: antigenic distinction from Norwalk and Mexico viruses. Clin Diagn Lab Immunol. 1999;6:142–145. doi: 10.1128/cdli.6.1.142-145.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Han MG, Smiley JR, Thomas C, Saif LJ. Genetic recombination between two genotypes of genogroup III bovine noroviruses (BoNVs) and capsid sequence diversity among BoNVs and Nebraska-like bovine enteric caliciviruses. J Clin Microbiol. 2004;42:5214–5224. doi: 10.1128/JCM.42.11.5214-5224.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Han MG, Wang Q, Smiley JR, Chang KO, Saif LJ. Self-assembly of the recom- binant capsid protein of a bovine norovirus (BoNV) into virus-like particles and evaluation of cross-reactivity of BoNV with human noroviruses. J Clin Microbiol. 2005;43:778–785. doi: 10.1128/JCM.43.2.778-785.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Humphrey W, Dalke A, Schulten K. VMD: visual molecular dynamics 1. J Mol Graph. 1996;14:33–38. doi: 10.1016/0263-7855(96)00018-5. [DOI] [PubMed] [Google Scholar]
- Jiang X, Graham DY, Wang KN, Estes MK. Norwalk virus genome cloning and characterization. Science. 1990;250:1580–1583. doi: 10.1126/science.2177224. [DOI] [PubMed] [Google Scholar]
- Jiang X, Wang M, Graham DY, Estes MK. Expression, self-assembly, and antigenicity of the Norwalk virus capsid protein. J Virol. 1992;66:6527–6532. doi: 10.1128/jvi.66.11.6527-6532.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jiang X, Cubitt D, Hu J, Dai X, Treanor J, Matson DO, Pickering LK. Development of an ELISA to detect MX virus, a human calicivirus in the snow Mountain agent genogroup. J Gen Virol. 1995;76:2739–2747. doi: 10.1099/0022-1317-76-11-2739. [DOI] [PubMed] [Google Scholar]
- Jiang X, Zhong WM, Farkas T, Huang PW, Wilton N, Barrett E, Fulton D, Morrow R, Matson DO. Baculovirus expression and antigenic characterization of the capsid proteins of three Norwalk-like viruses. Arch Virol. 2002;147:119–130. doi: 10.1007/s705-002-8306-5. [DOI] [PubMed] [Google Scholar]
- Karst SM, Wobus CE, Lay M, Davidson J, Virgin HW. STAT1-dependent innate immunity to a Norwalk-like virus. Science. 2003;299:1575–1578. doi: 10.1126/science.1077905. [DOI] [PubMed] [Google Scholar]
- Katayama K, Shirato-Horikoshi H, Kojima S, Kageyama T, Oka T, Hoshino F, Fukushi S, Shinohara M, Uchida K, Suzuki Y, Gojobori T, Takeda N. Phylogenetic analysis of the complete genome of 18 Norwalk-like viruses. Virology. 2002;299:225–239. doi: 10.1006/viro.2002.1568. [DOI] [PubMed] [Google Scholar]
- Labbe M, Charpilienne A, Crawford SE, Estes MK, Cohen J. Expression of rotavirus VP2 produces empty corelike particles. J Virol. 1991;65:2946–2952. doi: 10.1128/jvi.65.6.2946-2952.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lambden PR, Caul EO, Ashley CR, Clarke IN. Sequence and genome organization of a human small round-structured (Norwalk-like) virus. Science. 1993;259:516–519. doi: 10.1126/science.8380940. [DOI] [PubMed] [Google Scholar]
- Lindesmith L, Moe C, Lependu J, Frelinger JA, Treanor J, Baric RS. Cellular and humoral immunity following Snow Mountain virus challenge. J Virol. 2005;79:2900–2909. doi: 10.1128/JVI.79.5.2900-2909.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Liu BL, Lambden PR, Gunther H, Otto P, Elschner M, Clarke IN. Molecular characterization of a bovine enteric calicivirus: relationship to the Norwalk-like viruses. J Virol. 1999;73:819–825. doi: 10.1128/jvi.73.1.819-825.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lochridge VP, Hardy ME. Snow Mountain virus genome sequence and virus-like particle assembly. Virus Genes. 2003;26:71–82. doi: 10.1023/A:1022334323013. [DOI] [PubMed] [Google Scholar]
- Lole KS, Bollinger RC, Paranjape RS, Gadkari D, Kulkarni SS, Novak NG, Ingersoll R, Sheppard HW, Ray SC. Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. J Virol. 1999;73:152–160. doi: 10.1128/jvi.73.1.152-160.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mendez II, Hermann LL, Hazelton PR, Coombs KM. A comparative analysis of freon substitutes in the purification of reovirus and calicivirus. J Virol Methods. 2000;90:59–67. doi: 10.1016/S0166-0934(00)00217-2. [DOI] [PubMed] [Google Scholar]
- Noel JS, Ando T, Leite JP, Green KY, Dingle KE, Estes MK, Seto Y, Monroe SS, Glass RI. Correlation of patient immune responses with genetically characterized small round-structured viruses involved in outbreaks of nonbacterial acute gastroenteritis in the United States, 1990 to 1995. J Med Virol. 1997;53:372–383. doi: 10.1002/(SICI)1096-9071(199712)53:4<372::AID-JMV10>3.0.CO;2-H. [DOI] [PubMed] [Google Scholar]
- Oliver SL, Asobayire E, Dastjerdi AM, Bridger JC. 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. doi: 10.1016/j.virol.2006.02.027. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Oliver SL, Batten C, Deng Y, Elschner M, Otto P, Charpilienne A, Clarke IN, Bridger JC, Lambden P. Genotype-1 and genotype-2 bovine noroviruses are antigenically distinct but share a cross-reactive epitope with human noroviruses. J Clin Microbiol. 2006;44:992–998. doi: 10.1128/JCM.44.3.992-998.2006. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Oliver SL, Brown DW, Green J, Bridger JC. A chimeric bovine enteric calicivirus: evidence for genomic recombination in genogroup III of the Norovirus genus of the Caliciviridae. Virology. 2004;326:231–239. doi: 10.1016/j.virol.2004.06.010. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Oliver SL, Dastjerdi AM, Wong S, El Attar L, Gallimore C, Brown DW, Green J, Bridger JC. Molecular characterization of bovine enteric caliciviruses: a distinct third genogroup of noroviruses (Norwalk-like viruses) unlikely to be of risk to humans. J Virol. 2003;77:2789–2798. doi: 10.1128/JVI.77.4.2789-2798.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Prasad BV, Hardy ME, Dokland T, Bella J, Rossmann MG, Estes MK. X-ray crystallographic structure of the Norwalk virus capsid. Science. 1999;286:287–290. doi: 10.1126/science.286.5438.287. [DOI] [PubMed] [Google Scholar]
- Reynolds DJ, Morgan JH, Chanter N, Jones PW, Bridger JC, Debney TG, Bunch KJ. Microbiology of calf diarrhoea in southern Britain. Vet Rec. 1986;119:34–39. doi: 10.1136/vr.119.2.34. [DOI] [PubMed] [Google Scholar]
- Rockx BH, Bogers WM, Heeney JL, van Amerongen G, Koopmans MP. Experimental norovirus infections in non-human primates. J Med Virol. 2005;75:313–320. doi: 10.1002/jmv.20273. [DOI] [PubMed] [Google Scholar]
- Schmidt HA, Strimmer K, Vingron M, von Haeseler A. TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics. 2002;18:502–504. doi: 10.1093/bioinformatics/18.3.502. [DOI] [PubMed] [Google Scholar]
- Smiley JR, Hoet AE, Traven M, Tsunemitsu H, Saif LJ. Reverse transcription-PCR assays for detection of bovine enteric caliciviruses (BEC) and analysis of the genetic relationships among BEC and human caliciviruses. J Clin Microbiol. 2003;41:3089–3099. doi: 10.1128/JCM.41.7.3089-3099.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Snodgrass DR, Terzolo HR, Sherwood D, Campbell I, Menzies JD, Synge BA. Aetiology of diarrhoea in young calves. Vet Rec. 1986;119:31–34. doi: 10.1136/vr.119.2.31. [DOI] [PubMed] [Google Scholar]
- Someya Y, Takeda N, Miyamura T. Complete nucleotide sequence of the Chiba virus genome and functional expression of the 3C-like protease in Escherichia coli. Virology. 2000;278:490–500. doi: 10.1006/viro.2000.0672. [DOI] [PubMed] [Google Scholar]
- Staden R, Beal KF, Bonfield JK. The Staden package (1998) Methods Mol Biol. 2000;132:115–130. doi: 10.1385/1-59259-192-2:115. [DOI] [PubMed] [Google Scholar]
- Subekti DS, Tjaniadi P, Lesmana M, McArdle J, Iskandriati D, Budiarsa IN, Walujo P, Suparto IH, Winoto I, Campbell JR, Porter KR, Sajuthi D, Ansari AA, Oyofo BA. Experimental infection of Macaca nemestrina with a Toronto Norwalk-like virus of epidemic viral gastroenteritis. J Med Virol. 2002;66:400–406. doi: 10.1002/jmv.2159. [DOI] [PubMed] [Google Scholar]
- Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997;25:4876–4882. doi: 10.1093/nar/25.24.4876. [DOI] [PMC free article] [PubMed] [Google Scholar]
- van der Poel WH, van der Heide R, Verschoor F, Gelderblom H, Vinje J, Koopmans MP. Epidemiology of Norwalk-like virus infections in cattle in The Netherlands. Vet Microbiol. 2003;92:297–309. doi: 10.1016/S0378-1135(02)00421-2. [DOI] [PubMed] [Google Scholar]
- Wise AG, Monroe SS, Hanson LE, Grooms DL, Sockett D, Maes RK. Molecular characterization of noroviruses detected in diarrheic stools of Michigan and Wisconsin dairy calves: circulation of two distinct subgroups. Virus Res. 2004;100:165–177. doi: 10.1016/j.virusres.2003.11.014. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Woode GN, Bridger JC. Isolation of small viruses resembling astroviruses and caliciviruses from acute enteritis of calves. J Med Microbiol. 1978;11:441–452. doi: 10.1099/00222615-11-4-441. [DOI] [PubMed] [Google Scholar]
- Wyatt RG, Greenberg HB, Dalgard DW, Allen WP, Sly DL, Thornhill TS, Chanock RM, Kapikian AZ. Experimental infection of chimpanzees with the Norwalk agent of epidemic viral gastroenteritis. J Med Virol. 1978;2:89–96. doi: 10.1002/jmv.1890020203. [DOI] [PubMed] [Google Scholar]