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1 Institute for Virology and Antiviral Therapy, Hans-Knöll-Str. 2, 07745 Jena, Germany
2 Institute for Virus Diagnostics, Friedrich Loeffler Institute, Federal Research Institute for Animal Health, Boddenblick 5a, 17493 Insel Riems, Germany
3 School of Biology & Biochemistry, Medical Biology Centre, The Queen's University of Belfast, UK
Correspondence
Roland Zell
Roland.Zell{at}med.uni-jena.de
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The GenBank/EMBL/DDBJ accession numbers for the nucleotide sequences reported in the paper are DQ092769–DQ092795.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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). The classified animal enteroviruses include simian, porcine and bovine isolates. The first bovine enteroviruses were collected in the late 1950s (Kunin & Minuse, 1958; McFerran, 1958; Moll & Davis, 1959; see also: Barya et al., 1967; Dunne et al., 1974). They were isolated from (i) faeces of animals with symptoms of pneumonia, respiratory disease, enteritis, dysentery and fertility disorders, (ii) fetal fluids of an aborted calf, and (iii) the faeces of apparently healthy animals (Table 1). Difficulties in reproducing clinical symptoms, following experimental infection of animals, led to the conclusion that bovine enteroviruses were of only minor veterinary medical importance. Early attempts to classify bovine enteroviruses by serological means were reported by Huck & Cartwright (1964), Barya et al. (1967) and Dunne et al. (1974). In those studies seven, four and eight serogroups, respectively, were suggested. The proposal of Dunne et al. (1974) was approved by the WHO/FAO and prototype strains of seven serotypes were deposited in the ATCC, while the eighth serotype (designated PS 35) was subsequently found to be identical to PS 83, the proposed serotype 5. Later, this classification was revised following a proposal of Knowles & Barnett (1985). According to their work, bovine enteroviruses are classified into two serotypes, which are currently within the species Bovine enterovirus (BEV) of the genus Enterovirus (Stanway et al., 2005). However, after accumulation of enterovirus sequence data (Earle et al., 1988; McNally et al., 1994; McCarthy et al., 1999; Goens et al., 2004), concerns arose as to whether the present classification correctly represents the genetic diversity of bovine enteroviruses. In the present study, we sequenced six BEV strains that were collected in the USA (between 1957 and 1962) and deposited in the ATCC, as well as 11 recent field isolates from Germany (collected between 1982 and 2003). Among the American isolates are five of the previously suggested prototype strains. The sequence data were compared with published BEV sequences. Our genome data and subsequent phylogenetic analyses support the establishment of two BEV species, one of which contains two and the other three geno-/serotypes.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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. BEV strains PS 42 (VR-758), PS 83 (VR-757), PS 87 (VR-774) and PS 89 (VR-755) were obtained from the ATCC. LC-R4 was obtained from the National Veterinary Research Institute, Pulawy, Poland, and BEV-261 from the Institute for Animal Health (Pirbright, UK). Prior to RNA preparation, the viruses were propagated in Madin–Darby bovine kidney (MDBK) cells. This cell line was grown in Dulbecco's modified Eagle's medium supplemented with 10 % fetal bovine serum. Medium and supplements were obtained from Gibco-BRL Life Technologies.
Generation of BEV amplicons by long RT-PCR.
RNA of virus-infected MDBK cells was prepared by using the Perfect RNA kit of Eppendorf. Five micrograms of total RNA was reverse-transcribed with 20 pmol oligo(dT)20 primer and 40 U RevertAid H Minus M-MuLV reverse transcriptase (supplied by MBI Fermentas) in a total volume of 20 µl. Two microlitres of cDNA was used for PCR employing several primer sets. Different protocols were used depending on the expected size of the PCR product. For PCR products of approximately 1 kbp the following protocol was used: 0·2 mM each dNTP, 1 µM each primer, 10 mM Tris/HCl pH 8·3, 1·5 mM MgCl2, 50 mM KCl, 2·5 U Taq polymerase (total volume 50 µl). The PCR cycle was the same as used for routine diagnostics, i.e. 35 cycles of 50 s 94 °C, 50 s 55 °C, 1 min 72 °C. For the amplification of PCR products larger than 1·5 kbp, the Combizyme DNA polymerase mix supplied by InViTek was used. The PCR cycle was modified in the following way: 35 cycles of 30 s 92 °C, 50 s 55 °C, 8 min 68 °C. The 5'- and 3'-ends of the genomes were amplified using the 5'/3' RACE kit of Roche.
Sequencing of the BEV amplicons, sequence alignments and phylogenetic analysis.
PCR products were analysed by electrophoresis on agarose gels stained with ethidium bromide. PCR products of the expected size were purified by using either the QIAquick PCR Purification kit or the QIAquick Gel Extraction kit (Qiagen). Sequencing was performed according to the cycle sequencing protocol of ABI. The products were analysed on a Prism 310 Genetic Analyser of ABI. The sequences were aligned manually or with the help of CLUSTAL W (Thompson et al., 1994). Neighbour-joining trees were calculated with the quartet puzzling method (Strimmer & von Haeseler, 1996; Strimmer et al., 1997) using the JTT substitution model for amino acid sequences (Jones et al., 1992) and the Tamura–Nei model for nucleotide sequences (Tamura & Nei, 1993). The reliability of the clustering was tested by 10 000–25 000 iterations in the quartet puzzling method depending on the complexity of the dataset. For tree construction, maximum-likelihood branch lengths were computed. Consistency of branching was also tested with the maximum-parsimony algorithm using the PHYLIP program package (Felsenstein, 1995) and PROTML program (Adachi & Hasegawa, 1992).
RNA secondary predictions and free-energy calculations were performed with the MFOLD program (version 3.0; Zuker et al., 1999).
Nucleotide sequence accession numbers.
The nucleotide sequence data reported in this paper were submitted to the GenBank nucleotide sequence database (accession nos DQ092769–DQ092795, see also Table 2). For sequence alignments, available sequences of bovine, human, porcine and simian enteroviruses as well as human rhinoviruses were used (for the complete compilation of virus strains and GenBank accession numbers used see Supplementary Table; available in JGV Online).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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; McNally et al., 1994; McCarthy et al., 1999; Goens et al., 2004). Briefly, a long open reading frame encodes a polyprotein ranging from 2166 to 2176 aa. The sequences of the polymerase-encoding genome region, which are clearly distinct from the human enteroviruses, suggested the establishment of a discrete species named BEV. However, the low degree of sequence identity between the capsid protein sequences of strains VG(5)27, K 2577 and SL 305 (all serotype 1 according to the classification of Knowles & Barnett, 1985) and those of strains PS 87 and RM2 (both serotype 2) prompted us to study bovine enteroviruses in more detail. The aim of this study was to compare the complete sequences of representative strains of the seven serotypes previously proposed by Dunne et al. (1974). With the exception of BEV-165, which has been previously sequenced (M. McIlhatton, personal communication), all strains deposited in the ATCC by C. M. Kunin and H. W. Dunne were sequenced. This collection included five of the suggested prototype strains (BEV-261, PS 42, PS 83, PS 87 and PS 89) and LC-R4, which belongs to the same serogroup as BEV-1 and VG(5)27. Moreover, 11 German isolates collected between 1982 and 2003 were also included in this study. For the latter viruses, a minimum of the 5'-NTR, the P1 coding region, the 3D polymerase coding region and the 3'-NTR were sequenced. The BEV sequences were compared with representative human, porcine and simian enterovirus as well as with human rhinovirus sequences taken from the GenBank database (see Table 2).
In order to solve the question of whether there are one or more BEV species, the pairwise sequence relationships for each of the genome-encoded capsid proteins 1A–1D and 3D were calculated. In previous studies, this approach provided useful evidence for species distinction (Van Regenmortel et al., 1997; Zell et al., 2001). Three frequency peaks of amino acid identity scores are observed for the capsid proteins 1C and 1D, and two peaks for the 3D polymerase (Fig. 1). These distribution patterns indicate the existence of heterogeneous geno-/serotypes and a higher order taxon, presumably a species.
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). The 2C protein of the BEV cluster B is 1 aa shorter than the 2C of the A cluster.
The phylogenetic analysis of the P1 polyprotein included four HRV strains as outgroups (HRV2, 3, 9 and 14) and at least one member of each recognized enterovirus species. The phylogenetic tree reveals two rhinovirus clusters and nine enterovirus clusters (Fig. 2). These clusters represent two BEV clusters (designated BEV-A and BEV-B), as well as the acknowledged enterovirus species SEV-A, HEV-A to -D, PV and PEV, and the rhinovirus species HRV-A and -B. Each BEV cluster is further subdivided, presumably representing geno-/serotypes. In cluster A, group 1 composes strains D 14/3/96, Vir 404/03, LC-R4, VG(5)27, VD 2860/1-9, D 8/01, D 58/96-V2130 and E 6-82, and group 2 includes BEV-165 (M4), PS 42, PS 83, D 3/98, 56/59/1, SD 1182 II, D 14/1/96, SL 305 and K 2577. In cluster B, group 1 consists of BEV-261 (also known as M2) and RM2, group 2 includes PS 89, PS 87/Maryland, Wye-3A and Jena 38/02, whereas PS 87/Belfast is the only member of group 3. Genetic clustering of the BEV geno-/serotypes correlates in part with the former classification of Dunne et al. (1974) as LC-R4, BEV-261 (M2), BEV-165 (M4), PS 87/Belfast and PS 89 were previously described as discrete serotypes (see Table 2). However, PS 42 and PS 83, which were also described as discrete serotypes, are very similar to each other. One nucleotide insertion within the 5'-NTR and 33 nt substitutions (corresponding to 12 aa substitutions) were observed. Presumably, the substitutions reflect different passage histories of otherwise identical viruses. Moreover, both viruses are closely related to BEV-165, suggesting that they belong to the same geno-/serotype of the BEV-A cluster. BEV-261 (M2) and RM2 have very similar P1 sequences (Fig. 2) and are serologically almost indistinguishable (McNally et al., 1994). Obviously, these sequences represent different passage histories of the same virus.
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). Comparison of 1B and 1C indicates a similarity with geno-/serotype 2 of the BEV-A cluster. However, in the 1D comparison D 14/3/96 clusters with geno-/serotype 1 (Fig. 3). These findings are an indication of interserotypic recombination in the evolution of the BEVs. Another example of interserotypic recombination is PS 87/Belfast, which is closely related to BEV-B serotype 2 in the 1A region but is more related to BEV-261 (M2 and RM2) in the capsid proteins 1B–1D. An example of intraserotypic recombination is shown by LC-R4, which groups with Vir 404/03 in the 1B phylogeny and with VG(5)27 in the 1C and 1D phylogenies (Fig. 3). Besides these examples, incongruities between the 5'-NTR and 1A phylogenies on the one hand, and between 1D and 3D phylogenies on the other hand, indicate more frequent recombination events outside the capsid-encoding regions.
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), indicating the need to revise the present enterovirus taxonomy (see also Brown et al., 2003).
The phylogenetic analysis of the 3D polymerase included 72 rhinovirus and enterovirus sequences. The phylogenetic tree based on these sequences reveals genetic clusters representing species, whereas individual serotypes cannot be differentiated (Fig. 4). The BEV strains fall into two clusters correlating with clusters A and B of the P1 analysis. Again, CVA1, CVA19 and CVA22 separate from the remaining CVA strains (CVA11, 13, 15, 17, 18, 20, 21 and 24) and the polioviruses.
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) separated from the 5'-cloverleaf by a stem–loop, a small domain III and a less conserved domain VI (Zell & Stelzner, 1997). These structures are conserved among all sequenced BEV genomes. Phylogenetic analysis of 56 enteroviral 5'-NTR sequences revealed five clades correlating with five folding patterns of entero- and rhinoviral 5'-NTRs (Fig. 5 and Supplementary Figure in JGV Online). However, three of five groups (i.e. human enteroviruses, human rhinoviruses and bovine enteroviruses) contain more than one species.
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, upper panel) reveal a poliovirus-like folding pattern consisting of two stem–loop structures (domains X and Y), which have the potential to form a pseudoknot-like element (PKLE). Comparison of the tertiary structure models, based on the predicted secondary structures, show that the helices X and K (PKLE) are almost identical, while the Y helices of both clusters differ in length, in sequence and in the central base–base mismatch (Fig. 6, lower panel).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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suggested the existence of eight BEV serotypes. However, only seven representative viruses were deposited in the ATCC, while the eighth strain (designated PS 35) was subsequently found to be identical to PS 83, the proposed serotype 5 isolate. Later, this classification was revised following a proposal that BEVs fell into only two serotypes (Knowles & Barnett, 1985). Typing of the BEVs by serological means may be difficult due to significant cross-reaction of type-specific sera with other BEV types. After accumulation of BEV sequence data, concerns arose as to whether the concept of two serotypes within a single BEV species correctly reflects the genetic variability of these viruses. Comparison of the sequences from the capsid protein region revealed relatively low intertypic amino acid identities ranging from 72 to 76 % between the type 1 and type 2 strains [VG(5)27, BEV-165 vs PS 87, RM2] (Zell & Stelzner, 1997). In order to establish a molecular-based BEV classification, six of the former prototype strains collected in the USA between 1957 and 1962 as well as 11 German field isolates (collected between 1982 and 2003) were sequenced. These sequences were compared with available BEV sequences. The data revealed that the bovine enteroviruses compose two major clusters that are characterized by structural features and by levels of sequence identity. These clusters (designated BEV-A and -B) correlate with two ‘serotypes' as defined by Knowles & Barnett (1985). However, there are strong arguments supporting the hypothesis that both clusters represent species rather than serotypes: (i) structural features (lengths of proteins 1B, 1C, 1D, 2C and length of 3'-NTR) are correlated with the clusters BEV-A and -B. (ii) The distribution pattern of amino acid identity scores obtained after pairwise comparisons of capsid protein sequences consists of three peaks (Fig. 1). (iii) Phylogenetic analyses of the 3D polymerase reveals two clades – an observation that is confirmed by the discontinuous distribution pattern of the 3D amino acid identity scores (Figs 1 and 4).
Within each cluster, further subgrouping was observed in pairwise sequence comparisons and in the phylogenetic analyses. This subgrouping partly correlates to the serotyping previously proposed by Dunne et al. (1974). While LC-R4, BEV-261 (M2 or RM2), PS 87 and PS 89 represent four discrete geno-/serotypes, BEV-165 (M4), PS 42 and PS 83 are closely related and should be considered as strains of another fifth geno-/serotype. Moreover, PS 42 and PS 83 are almost identical, even though they were deposited in the ATCC as discrete serotypes.
Phylogenetic analyses of the 5'-NTR, single capsid proteins and the 3D polymerase provided evidence for interserotypic and intraserotypic recombination (Fig. 3). Intertypic recombination in poliovirus (Cammack et al., 1988; Lipskaya et al., 1991) and echovirus (Andersson et al., 2002) has been described previously. In general, incongruence between phylogenies of different genome regions are considered indicative of recombination events in enteroviruses (Santti et al., 1999; Lindberg et al., 2003).
It is a generally accepted concept that picornavirus serotypes are molecularly defined by the diversity of the capsid proteins, whereas the less diverse non-structural protein regions define an enterovirus species. Accordingly, amino acid identities of the BEV 1D protein ranged from 50 to 55 % for heterologous species, 70 to 85 % for heterologous serotypes/homologous species and were greater than 90 % for homologous serotypes (compare Fig. 1). For the 3D polymerase, the observed amino acid identities were greater than 95 % of heterologous serotypes/homologous species (Fig. 1). In this context, difficulties in typing the isolate D 14/3/96 may be explained by an interserotypic recombination event in the evolution of this virus. However, proof of this hypothesis requires the analysis of numerous virus isolates collected in close temporal and spatial proximity. With the exception of D 14/1/96, such virus isolates are not available. However, it is an interesting observation that D 14/1/96 and D 14/3/96 are closely related in their 5'-NTR and 3D gene region (Fig. 3). The capsid proteins of both isolates are considerably divergent. This suggests multiple recombination events in the evolution of these epidemiologically related viruses. A prerequisite of enterovirus recombination is the double/multiple infection of an individual host, which is common during vaccination with the live-attenuated polio vaccine but less frequent with non-polio enteroviruses.
Recently, Goens et al. (2004) published the genome sequences of PS 87/Maryland and Wye-3A. Both sequences cluster with PS 89 (Figs 2 and 3). Likewise, PS 87/Pirbright and PS 89 are identical (N. J. Knowles, personal communication). Instead, the sequence of PS 87/Belfast is identical to the previously published partial PS 87 sequence (GenBank accession no. X79368; McNally et al., 1994). It is noteworthy that the PS 87/Belfast and PS 89 strains used in the present study were directly received from the ATCC. Thus, one cannot exclude that, during the passage history of PS 87/Maryland and PS 87/Pirbright, this strain was mixed up with PS 89 or that virus stocks were mixtures of both viruses. (Indeed it is possible that some of the confusion presented by previous BEV serological classification studies have arisen by some virus isolates being mixtures of bovine enteroviruses).
Further analysis of the BEV genomes confirmed previous findings concerning the secondary structures of the 5'-NTR. The BEVs possess a second cloverleaf and characteristic RNA structures of the internal ribosome entry site as previously described (Zell & Stelzner, 1997; Zell et al., 1999). Krumbholz et al. (2002) have recently described five groups of entero- and rhinoviruses based on their predicted 5'-NTR folding patterns. Phylogenetic analysis of enteroviral and rhinoviral 5'-NTRs based on a representative number of sequences confirmed this observation (Fig. 5). Although characteristic for the BEVs, the 5'-NTR sequences are not a distinctive feature for species and serotype demarcation.
The 3'-NTR of the BEVs is poliovirus-like as suggested from the secondary structure predictions. It consists of two stem–loop structures (domains X and Y) allowing the formation of a PKLE. Tertiary structure models of representative BEV strains suggest that base stacking of helix X protrudes into the loop of the X domain, which forms helix K by base-pairing with the loop of the Y domain. This part of the 3'-NTR is almost identical in all sequenced BEVs (Fig. 6) and the porcine enteroviruses (data not shown), while the Y helix differs in these viruses.
Although enterovirus taxonomy was recently revised (King et al., 2000; Stanway et al., 2005), the present classification of the species Bovine enterovirus, Human enterovirus C and Poliovirus still appears to be inadequate. The sequencing data presented in this study support a revision of the present enterovirus taxonomy. According to our results, the bovine enteroviruses should be classified into two species (BEV-A and -B) containing at least two and three geno-/serotypes, respectively. Sequencing of further bovine, caprine and ovine enterovirus isolates may lead to the identification of additional geno-/serotypes. Like the human enteroviruses, most of the BEV isolates may unambiguously be typed by 1B, 1C or 1D gene regions, with the exception of isolate D 14/3/96. A more comprehensive set of sequence data may help to define subgenomic regions suited for the genotyping of BEV isolates.
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ACKNOWLEDGEMENTS |
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Received 29 June 2005;
accepted 12 October 2005.
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