Short communication Evidence for the porcine origin of equine rotavirus strain H-1 Souvik Ghosh *, Tsuzumi Shintani, Nobumichi Kobayashi Department of Hygiene, Sapporo Medical University School of Medicine, Sapporo, Japan 1. Introduction Equine group A rotavirus (RVA) is a major cause of severe diarrhea in foals (Browning and Begg, 1996; Collins et al., 2008; Imagawa et al., 1991; Saif et al., 1994). To date, RVAs are classified into at least 27 G and 35 P genotypes on the basis of differences in the nucleotide sequences of their outer capsid VP7 and VP4 genes, respectively (Matthijnssens et al., 2011a). Among them, G3P[12] and G14P[12] are regarded as the common equine RVA strains (Ciarlet et al., 1994; Collins et al., 2008; Elschner et al., 2005; Garaicoechea et al., 2011; Nemoto et al., 2011; Ntafis et al., 2010; Tsunemitsu et al., 2001). On the other hand, unusual RVA strains, such as G3P[3], G5P[7], G6P[1], G8P[1], G10P[1], G10P[11], G13P[18] strains, have also been detected in horses (Browning et al., 1991; Ciarlet et al., 2001; Garaicoechea et al., 2011; Imagawa et al., 1991, 1993; Is ˇa et al., 1996; Taniguchi et al., 1994). The G5 and P[7] RVA genotypes have been reported widely in pigs (Collins et al., 2010; Martella et al., 2010). Equine RVA strain H-1 (RVA/Horse-tc/GBR/H-1/1975/ G5P9[7]) was detected in a diarrheic stool sample collected from a young foal at a racing stable in United Kingdom in 1975 (Flewett et al., 1975), and isolated in AGMK and MA- 104 cells by Hoshino et al., 1983. Nucleotide sequencing of the partial genome (VP4, VP6–7, NSP1 and NSP4 genes), RNA–RNA hybridization and serological studies pointed towards the porcine origin of strain H-1 (Ciarlet et al., 2000, 2001; Flewett et al., 1975; Hoshino et al., 1983; Is ˇa and Snodgrass, 1994; Kojima et al., 1996; Matthijnssens et al., 2008; Taniguchi et al., 1994; Wu et al., 1993). However, whole genomic analysis of a RVA strain is essential to obtain conclusive information on its origin and evolution (Ghosh and Kobayashi, 2011; Matthijnssens et al., 2008, 2011a). Therefore, the nearly full-length nucleotide sequences (full-length sequences excluding the 5 0 - and 3 0 - end primer binding regions) of the remaining six gene segments (VP1–3, NSP2–3 and NSP5 genes) of strain H-1 were analyzed in the present study. Moreover, the previously reported nucleotide sequence of the NSP1 gene of strain H-1 (GenBank accession no. U23728, Kojima et al., Veterinary Microbiology 158 (2012) 410–414 A R T I C L E I N F O Article history: Received 5 January 2012 Received in revised form 8 February 2012 Accepted 23 February 2012 Keywords: Equine rotavirus Whole genomic analysis Porcine origin Interspecies transmission A B S T R A C T Equine group A rotavirus (RVA) strain H-1 (RVA/Horse-tc/GBR/H-1/1975/G5P9[7]) was found to have VP4, VP6-7, NSP1 and NSP4 genes of porcine origin. In order to obtain conclusive information on the exact origin and evolution of this unusual equine strain, the remaining six genes (VP1–3, NSP2–3 and NSP5 genes) of strain H-1 were analyzed in the present study. By whole genomic analysis, strain H-1 exhibited a porcine RVA-like genotype constellation (G5-P[7]-I5-R1-C1-M1-A8-N1-T1-E1-H1), different from those of typical equine RVA strains. The VP2–3 and NSP2–3 genes of strain H-1 were found to originate from porcine RVAs. On the other hand, it was difficult to pinpoint the exact origin of the VP1 and NSP5 genes of strain H-1, though phylogenetically, these genes appeared to be possibly derived from porcine or Wa-like human strains. Taken together, at least nine (VP2–4, VP6–7 and NSP1–4 genes) of the 11 gene segments of strain H-1 were found to be of porcine origin, revealing a porcine RVA-like genetic backbone. Therefore, strain H-1 is likely a porcine RVA strain that was transmitted to horses. ß 2012 Elsevier B.V. All rights reserved. * Corresponding author at: Department of Hygiene, Sapporo Medical University School of Medicine, S 1, W 17, Chuo-Ku, Sapporo, Hokkaido 060-8556, Japan. Tel.: +81 11 611 2111x2733; fax: +81 11 612 1660. E-mail addresses: [email protected], [email protected](S. Ghosh). Contents lists available at SciVerse ScienceDirect Veterinary Microbiology jou r nal h o mep ag e: w ww .els evier .co m/lo c ate/vetm ic 0378-1135/$ – see front matter ß 2012 Elsevier B.V. All rights reserved. doi:10.1016/j.vetmic.2012.02.037
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Introduction
Equine group A rotavirus (RVA) is a major cause of severearrhea in foals (Browning and Begg, 1996; Collins et al.,08; Imagawa et al., 1991; Saif et al., 1994). To date, RVAs aressified into at least 27 G and 35 P genotypes on the basis of
fferences in the nucleotide sequences of their outer capsid7 and VP4 genes, respectively (Matthijnssens et al., 2011a).ong them, G3P[12] and G14P[12] are regarded as the
mmon equine RVA strains (Ciarlet et al., 1994; Collins et al.,08; Elschner et al., 2005; Garaicoechea et al., 2011; Nemoto
al., 2011; Ntafis et al., 2010; Tsunemitsu et al., 2001). On theher hand, unusual RVA strains, such as G3P[3], G5P[7],P[1], G8P[1], G10P[1], G10P[11], G13P[18] strains, haveo been detected in horses (Browning et al., 1991; Ciarlet
al., 2001; Garaicoechea et al., 2011; Imagawa et al., 1991,93; Isa et al., 1996; Taniguchi et al., 1994). The G5 and P[7]
RVA genotypes have been reported widely in pigs (Collinset al., 2010; Martella et al., 2010).
Equine RVA strain H-1 (RVA/Horse-tc/GBR/H-1/1975/G5P9[7]) was detected in a diarrheic stool sample collectedfrom a young foal at a racing stable in United Kingdom in1975 (Flewett et al., 1975), and isolated in AGMK and MA-104 cells by Hoshino et al., 1983. Nucleotide sequencing ofthe partial genome (VP4, VP6–7, NSP1 and NSP4 genes),RNA–RNA hybridization and serological studies pointedtowards the porcine origin of strain H-1 (Ciarlet et al., 2000,2001; Flewett et al., 1975; Hoshino et al., 1983; Isa andSnodgrass, 1994; Kojima et al., 1996; Matthijnssens et al.,2008; Taniguchi et al., 1994; Wu et al., 1993). However,whole genomic analysis of a RVA strain is essential toobtain conclusive information on its origin and evolution(Ghosh and Kobayashi, 2011; Matthijnssens et al., 2008,2011a). Therefore, the nearly full-length nucleotidesequences (full-length sequences excluding the 50- and30- end primer binding regions) of the remaining six genesegments (VP1–3, NSP2–3 and NSP5 genes) of strain H-1were analyzed in the present study. Moreover, thepreviously reported nucleotide sequence of the NSP1 geneof strain H-1 (GenBank accession no. U23728, Kojima et al.,
R T I C L E I N F O
icle history:
ceived 5 January 2012
ceived in revised form 8 February 2012
cepted 23 February 2012
ywords:
uine rotavirus
hole genomic analysis
rcine origin
erspecies transmission
A B S T R A C T
Equine group A rotavirus (RVA) strain H-1 (RVA/Horse-tc/GBR/H-1/1975/G5P9[7]) was
found to have VP4, VP6-7, NSP1 and NSP4 genes of porcine origin. In order to obtain
conclusive information on the exact origin and evolution of this unusual equine strain, the
remaining six genes (VP1–3, NSP2–3 and NSP5 genes) of strain H-1 were analyzed in the
present study. By whole genomic analysis, strain H-1 exhibited a porcine RVA-like
genotype constellation (G5-P[7]-I5-R1-C1-M1-A8-N1-T1-E1-H1), different from those of
typical equine RVA strains. The VP2–3 and NSP2–3 genes of strain H-1 were found to
originate from porcine RVAs. On the other hand, it was difficult to pinpoint the exact origin
of the VP1 and NSP5 genes of strain H-1, though phylogenetically, these genes appeared to
be possibly derived from porcine or Wa-like human strains. Taken together, at least nine
(VP2–4, VP6–7 and NSP1–4 genes) of the 11 gene segments of strain H-1 were found to be
of porcine origin, revealing a porcine RVA-like genetic backbone. Therefore, strain H-1 is
likely a porcine RVA strain that was transmitted to horses.
� 2012 Elsevier B.V. All rights reserved.
Corresponding author at: Department of Hygiene, Sapporo Medical
iversity School of Medicine, S 1, W 17, Chuo-Ku, Sapporo, Hokkaido
S. Ghosh et al. / Veterinary Microbiology 158 (2012) 410–414 411
996) was found to lack three nucleotides in its putativepen reading frame (ORF), resulting in a NSP1 protein thatas one amino acid shorter than those of other RVA
trains. To confirm this observation, we repeated nucleo-de sequencing of the NSP1 gene of strain H-1.
. Materials and methods
The source of the tissue culture adapted isolate of strain-1 analyzed in the present study has been describedreviously (Wu et al., 1993). For RT-PCR, viral RNA wasxtracted from the tissue culture fluid of strain H-1 using theIAamp Viral RNA Mini kit (Qiagen Sciences, MD, USA). TheP1–3, NSP1–3 and NSP5 genes of strain H-1 were amplifiedsing primers reported previously (Ghosh et al., 2010a,b,011; Wang et al., 2010). Nucleotide sequences werebtained using the BigDye Terminator v3.1 Cycle Sequen-ing kit (Applied Biosystems, CA, USA) on an automated DNAequencer (ABI PRISM 3100). Sequence comparisons werearried out as described previously (Ghosh et al., 2010a,b).hylogenetic trees were constructed by the Neighbor-ining method (Saitou and Nei, 1987) using MEGA (v5.01)
oftware. The trees were statistically supported by boot-trapping with 1000 replicates, and phylogenetic distanceseasured by the Kimura two-parameter model. TheenBank accession numbers for the nucleotide sequencesf the VP1–3, NSP1–3 and NSP5 genes of strain H-1 are309138–JQ309144, respectively.
events are important to gain a proper understanding ofthe complex genetic diversity of RVAs (Ghosh andKobayashi, 2011; Martella et al., 2010). Moreover, novelRVA strains arising from these events may have the abilityto efficiently infect and spread among the population of thenew host, presenting a challenge to the efficacy of theexisting RVA vaccines (Palombo, 2003).
The VP4, VP6–7, NSP1 and NSP4 genes of equine RVAstrain H-1 were assigned to the P[7], I5, G5, A8 and E1genotypes, respectively (Matthijnssens et al., 2008). In thepresent study, the VP1–3, NSP2–3 and NSP5 genes of strainH-1 were assigned to the R1, C1, M1, N1, T1 and H1genotypes, respectively (Table 1). Taken together, strain H-1 was found to share 10 out of the 11 genotypes with thoseof typical porcine RVA strains RVA/Pig-tc/USA/OSU/1975/G5P9[7], RVA/Pig-xx/KOR/ PRG9121/2006/G9P[7] andRVA/Pig-tc/MEX/YM/1983/G11P9[7] (Table 1). Therefore,the overall genotype constellation of strain H-1 was foundto be porcine-like, different from those of other equine RVAstrains (Table 1).
In previous studies, the VP4, VP6–7, NSP1 and NSP4genes of equine RVA strain H-1 were shown to be derivedfrom porcine strains (Ciarlet et al., 2000, 2001; Kojimaet al., 1996; Matthijnssens et al., 2008; Taniguchi et al.,1994). Among the remaining six gene segments of strain H-1 analyzed in this study, the H-1 VP1 gene shared lownucleotide sequence identities (<90%) with those of otherRVA strains, and phylogenetically, clustered separately,near those of human G3P[8] strain RVA/Human-tc/JPN/ YO/1977/G3P1A[8], porcine-derived human strainRVA/Human-wt/NPL/KTM368/2004/G11P[25] (Matthijns-sens et al., 2010) and porcine strains PRG9121, RVA/Pig-xx/KOR/PRG942/2006/G9P[23] and RVA/Pig-xx/KOR/
able 1
enotype nature of the eleven gene segments of group A rotavirus (RVA) strain H-1 with those of selected RVA strains with known genomic constellations.
rey indicates the gene segments with a genotype identical to that of strain H-1. ‘‘–’’ indicates that no sequence data were available in the Gen Bank
atabase.
he species of origin of equine RVA strains are highlighted in bold.
Fig. 1. (A–F) Phylogenetic trees constructed from the nucleotide sequences of VP1–3, NSP2–3 and NSP5 genes of rotavirus strain RVA/Horse-tc/GBR/H-1/
1975/G5P9[7] with those of other RVA strains. Although strains representing all the RVA genotypes were included in the phylogenetic analyses to prepare
the dendograms, only those relevant to the present analysis are shown in (A)–(F). Within the R1, C1, M1, N1, T1 and H1 genotypes, clade/s consisting of
strains that are not directly related to the present study, but were included for unbiased analysis, have been compressed and labeled as subcluster/s. In all
trees, position of strain H-1 is highlighted by a dark circle. Bootstrap values less than 85% are not shown. Scale bar, 0.05 substitutions per nucleotide.
S. Ghosh et al. / Veterinary Microbiology 158 (2012) 410–414412
PH9cVtsmoBgIAwRb2gidpatSTsWsrwowOslo1wts
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S. Ghosh et al. / Veterinary Microbiology 158 (2012) 410–414 413
RG9235/ 2006/G9P[23] (Fig. 1A). The VP2 gene of strain-1 exhibited maximum nucleotide sequence identity of6.7% to that of porcine strain OSU, and phylogeneti-ally, both strains clustered together (Fig. 1B). The H-1P3 gene shared maximum genetic relatedness (nucleo-
ide sequence identity of 93.9%) with that of porcinetrain YM (Fig. 1C). The NSP2 gene of H-1 exhibitedaximum nucleotide sequence identity of 96.0% to that
f porcine-human reassortant strain RVA/Human-tc/RA/IAL28/1992/G5P[8] (Heiman et al., 2008). Phylo-enetically, the H-1 NSP2 gene clustered with strainL28, near porcine strains PRG9121 and PRG9235,ithin a cluster that also consisted of porcine strainVA/Pig-wt/IND/RU172/2002/G12P[7] and porcine-ovine reassortant strain RVA/Human-tc/CHN/R479/004/G4P[6] (Wang et al., 2010) (Fig. 1D). The NSP3ene of strain H-1 shared high nucleotide sequenceentities of 97.4%, 97.3% and 96.5% with those of
orcine strains RVA/Pig-tc/USA/SB1A/xxxx/G4P9[7], OSUnd RVA/Pig-tc/USA/Gottfried/1975/G4P[6], respec-ively, and phylogenetically, clustered near strainsB1A and Gottfried within a porcine cluster (Fig. 1E).he NSP5 gene of strain H-1 shared high nucleotideequence identities of 97–98% with several porcine and
a-like common human strains, such as G1, G9, G12trains, and phylogenetically, appeared to cluster sepa-ately between the human and porcine subclustersithin genotype H1 (Fig. 1F). The nucleotide sequence
f the NSP1 gene of strain H-1 determined in this studyas found to contain three additional nucleotides in itsRF (Supplementary Fig. S1), and the deduced protein
equence (486 amino acids long) was one amino acidnger than those reported previously (Kojima et al.,
996). Therefore, the putative NSP1 ORF of strain H-1as found to be of the same length (nt 32–nt 1492) as
hose of other RVAs, pointing towards a possibleequencing error in the previous study.
Taken together, at least nine (VP2–4, VP6–7 and NSP1– genes) of the 11 gene segments of strain H-1 were found
be of porcine origin, revealing a porcine RVA-like geneticackbone. On the other hand, it was difficult to pinpointe exact origin of the VP1 and NSP5 genes of strain H-1,ough phylogenetically, these genes appeared to be
ossibly derived from porcine or Wa-like human strains.ecently, the whole genomes of one unusual (G13P[18])nd six typical (G3P[12] and G14P[12]) equine RVA strainsave been analyzed (Matthijnssens et al., 2011b). Thepical equine RVA strains were found to exhibit a largely
onserved genetic constellation, which was highly diver-ent from those of strain H-1 (Table 1) and non-equine RVAtrains (Matthijnssens et al., 2011b). Therefore, strain H-1
likely a porcine RVA strain that was transmitted toorses. Although whole genomic analysis of RVA hasmerged as a reliable tool to obtain conclusive data onterspecies transmission events, this method has been
rimarily applied to the study of unusual human strainshosh and Kobayashi, 2011). However, as evident frome present study, whole genomic analysis of atypical
nimal RVAs might be equally important to study rare RVAterspecies transmission events involving different host
Conflict of interest
None.
Acknowledgement
The study was supported in part by the grant-in-aid forscientific research from the Ministry of Education, Culture,Sports, Science and Technology of Japan (Grant number22406017).
Appendix A. Supplementary data
Supplementary data associated with this article can befound, in the online version, at doi:10.1016/j.vet-mic.2012.02.037.
References
Browning, G.F., Chalmers, R.M., Fitzgerald, T.A., Snodgrass, D.R., 1991.Serological and genomic characterization of L338, a novel equinegroup A rotavirus G serotype. J. Gen. Virol. 72, 1059–1064.
Browning, G.F., Begg, A.P., 1996. Prevalence of G and P serotypes amongequine rotaviruses in the faeces of diarrhoeic foals. Arch. Virol. 141,1077–1089.
Ciarlet, M., Isa, P., Conner, M.E., Liprandi, F., 2001. Antigenic and molecularanalyses reveal that the equine rotavirus strain H-1 is closely relatedto porcine, but not equine, rotaviruses: interspecies transmissionfrom pigs to horses? Virus Genes 22, 5–20.
Ciarlet, M., Liprandi, F., Conner, M.E., Estes, M.K., 2000. Species specificityand interspecies relatedness of NSP4 genetic groups by comparativeNSP4 sequence analyses of animal rotaviruses. Arch. Virol. 145, 371–383.
Ciarlet, M., Reggeti, F., Pina, C.I., Liprandi, F., 1994. Equine rotaviruses withG14 serotype specificity circulate among Venezuelan horses. J. Clin.Microbiol. 32, 2609–2612.
Collins, P.J., Cullinane, A., Martella, V., O’Shea, H., 2008. Molecular char-acterization of equine rotavirus in Ireland. J. Clin. Microbiol. 46, 3346–3354.
Collins, P.J., Martella, V., Sleator, R.D., Fanning, S., O’Shea, H., 2010.Detection and characterisation of group A rotavirus in asymptomaticpiglets in southern Ireland. Arch. Virol. 155, 1247–1259.
Elschner, M., Schrader, C., Hotzel, H., Prudlo, J., Sachse, K., Eichhorn, W.,Herbst, W., Otto, P., 2005. Isolation and molecular characterisation ofequine rotaviruses from Germany. Vet. Microbiol. 105, 123–129.
Flewett, T.H., Bryden, A.S., Davies, H., 1975. Letter: virus diarrhoea in foalsand other animals. Vet. Rec. 96 JMM.
Garaicoechea, L., Mino, S., Ciarlet, M., Fernandez, F., Barrandeguy, M.,Parreno, V., 2011. Molecular characterization of equine rotavirusescirculating in Argentinean foals during a 17-year surveillance period(1992–2008). Vet. Microbiol. 148, 150–160.
Ghosh, S., Adachi, N., Gatheru, Z., Nyangao, J., Yamamoto, D., Ishino, M.,Urushibara, N., Kobayashi, N., 2011. Whole-genome analysis revealsthe complex evolutionary dynamics of Kenyan G2P[4] human rota-virus strains. J. Gen. Virol. 92, 2201–2208.
Ghosh, S., Alam, M.M., Ahmed, M.U., Talukdar, R.I., Paul, S.K., Kobayashi,N., 2010a. The complete genome constellation of a caprine group Arotavirus strain reveals common evolution with ruminant and humanrotavirus strains. J. Gen. Virol. 91, 2367–2373.
Ghosh, S., Kobayashi, N., 2011. Whole-genomic analysis of rotavirusstrains: current status and future prospects. Future Microbiol. 6,1049–1065.
Ghosh, S., Kobayashi, N., Nagashima, S., Chawla-Sarkar, M., Krishnan, T.,Ganesh, B., Naik, T.N., 2010b. Full genomic analysis and possibleorigin of a porcine G12 rotavirus strain RU172. Virus Genes 40,382–388.
Heiman, E.M., McDonald, S.M., Barro, M., Taraporewala, Z.F., Bar-Magen,T., Patton, J.T., 2008. Group A human rotavirus genomics: evidencethat gene constellations are influenced by viral protein interactions. J.Virol. 82, 11106–11116.
S. Ghosh et al. / Veterinary Microbiology 158 (2012) 410–414414
agawa, H., Sekiguchi, K., Anzai, T., Fukunaga, Y., Kanemaru, T., Ohishi,H., Higuchi, T., Kamada, M., 1991. Epidemiology of equine rotavirusinfection among foals in the breeding region. J. Vet. Med. Sci. 53,1079–1080.
agawa, H., Tanaka, T., Sekiguchi, K., Fukunaga, Y., Anzai, T., Minamoto,N., Kamada, M., 1993. Electropherotypes, serotypes, and subgroups ofequine rotaviruses isolated in Japan. Arch. Virol. 131, 169–176.
, P., Snodgrass, D.R., 1994. Serological and genomic characterization ofequine rotavirus VP4 proteins identifies three different P serotypes.Virology 201, 364–372.
, P., Wood, A.R., Netherwood, T., Ciarlet, M., Imagawa, H., Snodgrass,D.R., 1996. Survey of equine rotaviruses shows conservation of one Pgenotype in background of two G genotypes. Arch. Virol. 141, 1601–1612.
jima, K., Taniguchi, K., Kobayashi, N., 1996. Species-specific and inter-species relatedness of NSP1 sequences in human, porcine, bovine,feline, and equine rotavirus strains. Arch. Virol. 141, 1–12.
rtella, V., Banyai, K., Matthijnssens, J., Buonavoglia, C., Ciarlet, M., 2010.Zoonotic aspects of rotaviruses. Vet. Microbiol. 140, 246–255.
tthijnssens, J., Ciarlet, M., Heiman, E., Arijs, I., Delbeke, T., McDonald,S.M., Palombo, E.A., Gomara, M.I., Maes, P., Patton, J.T., Rahman, M.,Ranst, M.V., 2008. Full genome-based classification of rotavirusesreveals a common origin between human Wa-like and porcine rota-virus strains and human DS-1-like and bovine rotavirus strains. J.Virol. 82, 3204–3219.
tthijnssens, J., Ciarlet, M., McDonald, S.M., Attoui, H., Banyai, K., Brister,J.R., Buesa, J., Esona, M.D., Estes, M.K., Gentsch, J.R., Iturriza-Gomara, M.,Johne, R., Kirkwood, C.D., Martella, V., Mertens, P.P., Nakagomi, O.,Parreno, V., Rahman, M., Ruggeri, F.M., Saif, L.J., Santos, N., Steyer, A.,Taniguchi, K., Patton, J.T., Desselberger, U., Van Ranst, M., 2011a. Uni-formity of rotavirus strain nomenclature proposed by the RotavirusClassification Working Group (RCWG). Arch. Virol. 156, 1397–1413.
tthijnssens, J., Mino, S., Papp, H., Potgieter, C., Novo, L., Heylen, E.,Zeller, M., Garaicoeachea, L., Badaracco, A., Lengyel, G., Kisfali, P.,Collins, P., Ciarlet, M., O’Shea, H., Parreno, V., Banyai, K., Barrandeguy,M., Van Ranst, M., 2011b. Complete molecular genome analyses ofequine rotavirus A strains from different continents reveal several
new genotypes and a largely conserved genotype constellation. J. Gen.Virol., doi:10.1099/vir.0.039255-0.
Matthijnssens, J., Rahman, M., Ciarlet, M., Zeller, M., Heylen, E., Nakagomi,T., Uchida, R., Hassan, Z., Azim, T., Nakagomi, O., Van Ranst, M., 2010.Reassortment of human rotavirus gene segments into G11 rotavirusstrains. Emerg. Infect. Dis. 16, 625–630.
Nemoto, M., Tsunemitsu, H., Imagawa, H., Hata, H., Higuchi, T., Sato, S.,Orita, Y., Sugita, S., Bannai, H., Tsujimura, K., Yamanaka, T., Kondo, T.,Matsumura, T., 2011. Molecular characterization and analysis ofequine rotavirus circulating in Japan from 2003 to 2008. Vet. Micro-biol. 152, 67–73.
Ntafis, V., Fragkiadaki, E., Xylouri, E., Omirou, A., Lavazza, A., Martella, V.,2010. Rotavirus-associated diarrhoea in foals in Greece. Vet. Micro-biol. 144, 461–465.
Palombo, E.A., 2003. Interspecies transmission of rotavirus. In: Kobayashi,N. (Ed.), Genomic Diversity and Molecular Epidemiology of Rota-viruses. Research Signpost, Trivandrum, India, pp. 1–16.
Saif, L., Rosen, B., Parwani, A., 1994. Animal rotaviruses. In: Kapikian, A.Z.(Ed.), Virus Infections of the Gastrointestinal Tract. Marcel-Dekker,New York, pp. 279–367.
Saitou, N., Nei, M., 1987. The neighbor-joining method: a new method forreconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406–425.
Taniguchi, K., Urasawa, T., Urasawa, S., 1994. Species specificity andinterspecies relatedness in VP4 genotypes demonstrated by VP4sequence analysis of equine, feline, and canine rotavirus strains.Virology 200, 390–400.
Tsunemitsu, H., Imagawa, H., Togo, M., Shouji, T., Kawashima, K., Horino,R., Imai, K., Nishimori, T., Takagi, M., Higuchi, T., 2001. Predominanceof G3B and G14 equine group A rotaviruses of a single VP4 serotype inJapan. Arch. Virol. 146, 1949–1962.
Wang, Y.H., Kobayashi, N., Nagashima, S., Zhou, X., Ghosh, S., Peng, J.S., Hu,Q., Zhou, D.J., Yang, Z.Q., 2010. Full genomic analysis of a porcine-bovine reassortant G4P[6] rotavirus strain R479 isolated from aninfant in China. J. Med. Virol. 82, 1094–1102.
Wu, H., Taniguchi, K., Urasawa, T., Urasawa, S., 1993. Genomic relatednessof five equine rotavirus strains with different G serotype and P typespecificities. Res. Virol. 144, 455–464.
