[en] Bovine noroviruses are enteric pathogens that are detected in stool samples from cattle. Five genogroups are currently described in the genus Norovirus (family Caliciviridae), and within the genogroups, sequences are further divided into genotypes according to genetic homology and phylogenetic relationships. In this study, stool specimens from Belgian cattle were screened by RT-PCR. All of the sequences that were detected were phylogenetically related to genogroup III genotype 2 bovine noroviruses, confirming their higher prevalence in comparison with strains from genotype 1. When other sequences from around the world were introduced, phylogenetic inferences allowed neither the determination of phylogenetic lineages over time nor the deduction of topotypes for genotype 2 bovine noroviruses. Three complete genotype 2 bovine norovirus sequences were also compared genetically (Newbury2/1976 /UK, Dumfries/1994/UK and B309/2003/BE). Interestingly, the genetic divergence of the complete genomes of these three strains was relatively low, but a region of the N-terminal protein encoded by ORF1, the hypervariable region of the capsid gene encoded by ORF2, and a region of the minor structural protein encoded by ORF3 seem to be the most exposed to genetic evolution. Bayesian inference also showed that genetic evolution of genogroup III, genotype 2 bovine noroviruses over a 30-year period seemed to be lower than that already reported for noroviruses from the genotypes 3 and 4 in genogroup II.
Disciplines :
Veterinary medicine & animal health
Author, co-author :
Mauroy, Axel ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires > Virologie vétérinaire et maladies virales animales
Daube, Georges ; Université de Liège - ULiège > Département de sciences des denrées alimentaires > Microbiologie des denrées alimentaires
Thiry, Etienne ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires > Virologie vétérinaire et maladies virales animales
Language :
English
Title :
Genetic and evolutionary perspectives on genogroup III, genotype 2 bovine noroviruses
Alcala AC, Hidalgo MA, Obando C, Vizzi E, Liprandi F, Ludert JE (2003) Molecular identification of bovine enteric calciviruses in Venezuela. Acta Cient Venez 54: 148-152.
Bertolotti-Ciarlet A, Crawford SE, Hutson AM, Estes MK (2003) The 3' end of Norwalk virus mRNA contains determinants that regulate the expression and stability of the viral capsid protein VP1: a novel function for the VP2 protein. J Virol 77: 11603-11615.
Bok K, Abente EJ, Realpe-Quintero M, Mitra T, Sosnovtsev SV, Kapikian AZ, Green KY (2009) Evolutionary dynamics of GII. 4 noroviruses over a 34-year period. J Virol 83: 11890-11901.
Boon D, Mahar JE, Abente EJ, Kirkwood CD, Purcell RH, Kapikian AZ, Green KY, Bok K (2011) Comparative evolution of GII. 3 and GII. 4 norovirus over a 31-year period. J Virol 85: 8656-8666.
Bull RA, Tanaka MM, White PA (2007) Norovirus recombination. J Gen Virol 88: 3347-3359.
Bull RA, White PA (2011) Mechanisms of GII. 4 norovirus evolution. Trends Microbiol 19: 233-240.
Cannon JL, Lindesmith LC, Donaldson EF, Saxe L, Baric RS, Vinje J (2009) Herd immunity to GII. 4 noroviruses is supported by outbreak patient sera. J Virol 83: 5363-5374.
Deng Y, Batten CA, Liu BL, Lambden PR, Elschner M, Gunther H, Otto P, Schnurch P, Eichhorn W, Herbst W, Clarke IN (2003) Studies of epidemiology and seroprevalence of bovine noroviruses in Germany. J Clin Microbiol 41: 2300-2305.
Dingle KE (2004) Mutation in a Lordsdale norovirus epidemic strain as a potential indicator of transmission routes. J Clin Microbiol 42: 3950-3957.
Domingo E, Holland JJ (1997) RNA virus mutations and fitness for survival. Annu Rev Microbiol 51: 151-178.
Drummond AJ, Rambaut A, Shapiro B, Pybus OG (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22: 1185-1192.
Drummond AJ, Ho SY, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4: e88.
Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7: 214.
Duffy S, Shackelton LA, Holmes EC (2008) Rates of evolutionary change in viruses: patterns and determinants. Nat Rev Genet 9: 267-276.
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41: 95-98.
Jiang X, Wang M, Wang K, Estes MK (1993) Sequence and genomic organization of Norwalk virus. Virology 195: 51-61.
Kaplon J, Guenau E, Asdrubal P, Pothier P, Ambert-Balay K (2011) Possible novel nebovirus genotype in cattle, France. Emerg Infect Dis 17: 1120-1123.
Lepage T, Bryant D, Philippe H, Lartillot N (2007) A general comparison of relaxed molecular clock models. Mol Biol Evol 24: 2669-2680.
Li WL, Drummond AJ (2012) Model averaging and Bayes factor calculation of relaxed molecular clocks in Bayesian phylogenetics. Mol Biol Evol 29: 751-761.
Lindesmith LC, Donaldson EF, Lobue AD, Cannon JL, Zheng DP, Vinje J, Baric RS (2008) Mechanisms of GII. 4 norovirus persistence in human populations. PLoS Med 5: e31.
Lindesmith LC, Costantini V, Swanstrom J, Debbink K, Donaldson EF, Vinje J, Baric RS (2013) Emergence of a norovirus GII. 4 strain correlates with changes in evolving blockade epitopes. J Virol 87: 2803-2813.
Liu BL, Lambden PR, Gunther H, Otto P, Elschner M, Clarke IN (1999) Molecular characterization of a bovine enteric calicivirus: relationship to the Norwalk-like viruses. J Virol 73: 819-825.
Lochridge VP, Hardy ME (2007) A single-amino-acid substitution in the P2 domain of VP1 of murine norovirus is sufficient for escape from antibody neutralization. J Virol 81: 12316-12322.
Mathijs E, Muylkens B, Mauroy A, Ziant D, Delwiche T, Thiry E (2010) Experimental evidence of recombination in murine noroviruses. J Gen Virol 91: 2723-2733.
Mauroy A, Scipioni A, Mathijs E, Saegerman C, Mast J, Bridger JC, Ziant D, Thys C, Thiry E (2009) Epidemiological study of bovine norovirus infection by RT-PCR and a VLP-based antibody ELISA. Vet Microbiol 137: 243-251.
Mauroy A, Scipioni A, Mathijs E, Thys C, Thiry E (2009) Molecular detection of kobuviruses and recombinant noroviruses in cattle in continental Europe. Arch Virol 154: 1841-1845.
Mauroy A, Gillet L, Mathijs E, Vanderplasschen A, Thiry E (2011) Alternative attachment factors and internalisation pathways for GIII. 2 bovine noroviruses. J Gen Virol 92: 1398-1409.
Mauroy A, Scipioni A, Mathijs E, Ziant D, Daube G, Thiry E (2012) Complete genome sequence of a novel bovine norovirus: evidence for slow genetic evolution in genogroup III genotype 2 noroviruses. J Virol 86: 12449-12450.
McFadden N, Bailey D, Carrara G, Benson A, Chaudhry Y, Shortland A, Heeney J, Yarovinsky F, Simmonds P, Macdonald A, Goodfellow I (2011) Norovirus regulation of the innate immune response and apoptosis occurs via the product of the alternative open reading frame 4. PLoS Pathog 7: e1002413.
Mijovski JZ, Poljsak-Prijatelj M, Steyer A, Barlic-Maganja D, Koren S (2010) Detection and molecular characterisation of noroviruses and sapoviruses in asymptomatic swine and cattle in Slovenian farms. Infect Genet Evol 10: 413-420.
Milnes AS, Binns SH, Oliver SL, Bridger JC (2007) Retrospective study of noroviruses in samples of diarrhoea from cattle, using the Veterinary Laboratories Agency's Farmfile database. Vet Rec 160: 326-330.
Oliver SL, Dastjerdi AM, Wong S, El-Attar L, Gallimore C, Brown DW, Green J, Bridger JC (2003) Molecular characterization of bovine enteric caliciviruses: a distinct third genogroup of noroviruses (Norwalk-like viruses) unlikely to be of risk to humans. J Virol 77: 2789-2798.
Oliver SL, Asobayire E, Dastjerdi AM, Bridger JC (2006) Genomic characterization of the unclassified bovine enteric virus Newbury agent-1 (Newbury1) endorses a new genus in the family Caliciviridae. Virology 350: 240-250.
Oliver SL, Asobayire E, Charpilienne A, Cohen J, Bridger JC (2007) Complete genomic characterization and antigenic relatedness of genogroup III, genotype 2 bovine noroviruses. Arch Virol 152: 257-272.
Park SI, Jeong C, Kim HH, Park SH, Park SJ, Hyun BH, Yang DK, Kim SK, Kang MI, Cho KO (2007) Molecular epidemiology of bovine noroviruses in South Korea. Vet Microbiol 124: 125-133.
Reuter G, Pankovics P, Egyed L (2009) Detection of genotype 1 and 2 bovine noroviruses in Hungary. Vet Rec 165: 537-538.
Scipioni A, Mauroy A, Vinje J, Thiry E (2008) Animal noroviruses. Vet J 178: 32-45.
Seah EL, Gunesekere IC, Marshall JA, Wright PJ (1999) Variation in ORF3 of genogroup 2 Norwalk-like viruses. Arch Virol 144: 1007-1014.
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
van Der Poel WH, van der Heide R, Verschoor F, Gelderblom H, Vinje J, Koopmans MP (2003) Epidemiology of Norwalk-like virus infections in cattle in The Netherlands. Vet Microbiol 92: 297-309.
Vinje J, Hamidjaja RA, Sobsey MD (2004) Development and application of a capsid VP1 (region D) based reverse transcription PCR assay for genotyping of genogroup I and II noroviruses. J Virol Methods 116: 109-117.
Wise AG, Monroe SS, Hanson LE, Grooms DL, Sockett D, Maes RK (2004) Molecular characterization of noroviruses detected in diarrheic stools of Michigan and Wisconsin dairy calves: circulation of two distinct subgroups. Virus Res 100: 165-177.
Woode GN, Bridger JC (1978) Isolation of small viruses resembling astroviruses and caliciviruses from acute enteritis of calves. J Med Microbiol 11: 441-452.
Yilmaz H, Turan N, Altan E, Bostan K, Yilmaz A, Helps CR, Cho KO (2011) First report on the phylogeny of bovine norovirus in Turkey. Arch Virol 156: 143-147.
Zakhour M, Ruvoen-Clouet N, Charpilienne A, Langpap B, Poncet D, Peters T, Bovin N, Le Pendu J (2009) The alphaGal epitope of the histo-blood group antigen family is a ligand for bovine norovirus Newbury2 expected to prevent cross-species transmission. PLoS Pathog 5: e1000504.
Zheng DP, Ando T, Fankhauser RL, Beard RS, Glass RI, Monroe SS (2006) Norovirus classification and proposed strain nomenclature. Virology 346: 312-323.