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1 Department of Microbiology, College of Medicine, Korea University, Seoul, Korea
2 Bank for Pathogenic Viruses, Korea University, Seoul, Korea
3 Force Health Protection, 18th Medical Command, Unit 15281, APO AP 96205, Korea
4 5th Medical Detachment, 168th Medical Battalion (Area Support), 18th Medical Command, Unit 15247, APO AP 96205, Korea
5 Virology Division, US Army Medical Research Institute of Infectious Diseases, Frederick, MD, USA
6 Department of Pediatrics, John A. Burns School of Medicine, University of Hawaii at Manoa, Honolulu, HI, USA
Correspondence
Jin-Won Song
jwsong{at}korea.ac.kr
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Present address: College of Medicine, Kangwon National University, Chuncheon, Korea. 
The GenBank/EMBL/DDBJ accession numbers for the S and M genomic sequences of Muju virus determined in this study are DQ138125, DQ138127–DQ138144 and EF198313.
A supplementary table showing oligonucleotide primers for amplification of the S and M segments of MUJV is available with the online version of this paper.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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). Since that time, several hundred HFRS cases (with mortality rates of 4–8 %) have been reported annually among military personnel and civilians in Korea. The majority of these clinically severe HFRS cases in Korea are caused by Hantaan virus (HTNV), originally isolated from lung tissue of the striped field mouse (Apodemus agrarius) captured in Songnae-ri, Gyeonggi province, Korea (Lee et al., 1978), and Seoul virus (SEOV), harboured by the Norway rat (Rattus norvegicus) (Lee et al., 1982). Soochong virus (SOOV), recently isolated from the Korean field mouse (Apodemus peninsulae), also accounts for cases of HFRS (Baek et al., 2006). By contrast, the bank vole (Myodes glareolus, formerly Clethrionomys glareolus), which serves as the reservoir host of Puumala virus (PUUV), the cause of a milder form of HFRS (known as nephropathia epidemica) throughout Scandinavia and Europe (Brummer-Korvenkontio et al., 1980; Yanagihara et al., 1984), is absent in Korea. Nevertheless, approximately 7 % of HFRS cases in Korea exhibit fourfold or higher antibody titres to PUUV than to HTNV by double-sandwich IgM capture ELISA. Based on these ‘atypical’ ELISA reactivities, the existence of one or more antigenically distinct, arvicolid rodent-borne hantaviruses has long been suspected in the Korean Peninsula. By analysing the phylogenetic relationships between Myodes glareolus and other arvicolid rodents, the royal vole (Myodes regulus, formerly Eothenomys regulus) appeared to be a likely candidate as a reservoir of a PUUV-related hantavirus in Korea. Using RT-PCR, a genetically distinct arvicolid rodent-borne hantavirus, designated Muju virus (MUJV), was detected in the tissues of Myodes regulus captured in widely separated geographical regions in Korea during 1996–2007. The discovery of MUJV adds to the growing list of hantaviruses in Korea and may account for HFRS cases that cannot be attributed to HTNV, SOOV or SEOV infection.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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; Fig. 1). Lung and spleen tissues of royal voles, collected with separate sterile instruments, were frozen at –70 °C until used for gene amplification and virus isolation.
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). In addition, sera from IFA-seropositive voles were tested for neutralizing antibodies against PUUV, HTNV, SEOV and Prospect Hill virus (PHV) by a plaque-reduction neutralization test (PRNT) (Baek et al., 2006; Lee et al., 1985). Briefly, serial twofold dilutions of sera from royal voles captured in Jeollabuk and Gangwon provinces were incubated with 50–100 p.f.u. PUUV, PHV, HTNV or SEOV at 4 °C overnight. Thereafter, virus/serum mixtures were inoculated onto confluent monolayers of Vero E6 cells (ATCC CRL-1586) grown in 96-well flat-bottomed tissue culture plates, adsorbed at 37 °C for 1 h and then overlaid with Dulbecco's modified Eagle's medium (DMEM) containing 0.7 % methylcellulose (Sigma). After incubation for 7 (HTNV and SEOV) or 14 (PUUV and PHV) days, monolayers were fixed with 2 % paraformaldehyde and plaques were counted after immunostaining with rat antiserum against the respective hantavirus and horseradish peroxidase-conjugated goat anti-rat IgG and diaminobenzidine (0.7 mg ml–1). PRNT titres were expressed as the reciprocal of the highest serum dilution giving an 80 % reduction.
Virus isolation.
Subconfluent monolayers of Vero E6 cells were inoculated with 5 % suspensions of Myodes regulus lung and spleen tissue in which MUJV sequences were detected by RT-PCR. Inocula were adsorbed by centrifugation at 670 g for 2 h at 25 °C. Subsequently, cells were maintained in DMEM supplemented with 5 % heat-inactivated fetal bovine serum and subcultured at 10- to 14-day intervals, at which time cells were examined for hantavirus antigens by IFA test, using convalescent-phase sera from HFRS patients and rat and mouse antisera specific for PUUV. Vero E6 cells at each passage were also examined for MUJV sequences by RT-PCR. In further experiments, suckling Mongolian gerbils (Meriones unguiculatus) were inoculated by the intraperitoneal route with tissue homogenates (Yanagihara et al., 1985) and their tissues analysed for MUJV sequences by RT-PCR.
RT-PCR amplification of hantavirus.
Total RNA, extracted from 20–50 mg of each lung tissue of PUUV-seropositive Myodes regulus using RNAzol (Gibco-BRL), was reverse transcribed using a Superscript II RNase H– reverse transcriptase kit (Gibco-BRL). Hantavirus sequences were then amplified using newly designed and previously described (S+20, M+1) oligonucleotide primers (see Supplementary Table S1, available in JGV Online) (Song et al., 2004; Baek et al., 2006). Gene amplification reactions were performed in 50 µl reaction mixtures containing 200 mM dNTPs, 0.5 U Supertherm polymerase (PureTech Co.), 1 µg cDNA and 10 pM each primer. Initial denaturation at 98 °C for 5 min was followed by touchdown cycling with denaturation at 98 °C for 1 min, annealing from 48 to 38 °C for 1 min and elongation at 72 °C for 1 min 30 s, followed by 20 cycles of denaturation at 98 °C for 1 min, annealing at 42 °C for 1 min and elongation at 72 °C for 1 min 30 s in a Mastercycler ep gradient S (Eppendorf AG). PCR products were size fractionated by electrophoresis on 1–1.5 % agarose gels containing ethidium bromide at 0.5 mg ml–1 and purified using a Wizard PCR Preps DNA Purification System (Promega). DNA sequencing was performed in both directions using a dye-termination cycle-sequencing ready reaction kit (Applied Biosystems) on an automated sequencer (model 377, Perkin Elmer).
PCR amplification of mitochondrial DNA.
Total DNA was extracted from fresh vole liver tissue using a QIAamp tissue kit (Qiagen). To study the phylogenetic relationship of Myodes regulus from various geographical regions in Korea, the cytochrome b region of mtDNA was amplified by PCR using previously described universal primers that amplify a 482 bp product: +L14115 (5'-CGAAGCTTGATATGAAAAACCATCGTTG-3'); and –L14532 (5'-GCAGCCCCTCAGAATGATATTTGTCCAC-3') (Smith & Patton, 1991). PCR was performed in 50 µl reaction mixtures containing 200 µM dNTP and 1.25 U rTaq polymerase (Takara). The initial denaturation step was at 95 °C for 4 min, followed by 40 cycles of denaturation at 94 °C for 1 min, annealing at 55 °C for 1 min and elongation at 72 °C for 1 min in a PTC-200 DNA Engine Peltier thermal cycler (MJ Research). Amplicons were cloned using the pSTBlue-1 vector (Novagen) and sequenced as described above.
Phylogenetic analysis.
MUJV sequences from 13 royal voles were aligned and compared with previously published sequences of PUUV strains (Horling et al., 1995; Lundkvist et al., 1998; Plyusnin et al., 1994b; Reip et al., 1995; Sironen et al., 2001; Xiao et al., 1993) and other arvicolid rodent-borne hantaviruses, including PUUV-related viruses (Tobetsu) from Myodes rufocanus in Hokkaido, Japan (Kariwa et al., 1995), Khabarovsk virus (KHAV) from Microtus fortis (Horling et al., 1996), and Tula virus (TULV) from Microtus arvalis (Plyusnin et al., 1994a; Song et al., 2004) and Pitymys subterraneus (Song et al., 2002). Alignment of the full-length S and M genomic segments was carried out using CLUSTAL W (Lasergene program version 5; DNASTAR). For phylogenetic analysis, the neighbour-joining and maximum-parsimony methods (PAUP version 4.0; Sinauer Associates) were used (Swofford, 2003). Topologies were evaluated by bootstrap analysis of 1000 iterations.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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). The IFA seropositivity rates were 13.8 % (15/108) and 9.3 % (25/268) in Myodes regulus captured in Jeollabuk and Gangwon provinces, respectively. None of the 63 Myodes regulus captured in the other four provinces had serological evidence of hantavirus infection. Multiple attempts to isolate MUJV in Vero E6 cell cultures and in Mongolian gerbils were unsuccessful. However, in tests of sera from anti-PUUV IFA-positive Myodes regulus, captured in Jeollabuk and Gangwon provinces, for neutralizing antibodies against PUUV, PHV, HTNV and SEOV, PRNT titres against PUUV were consistently two- to sixfold higher (reciprocal titres of 320–1280), supporting the existence of a PUUV-like hantavirus.
Sequence analysis of MUJV
Genetically distinct hantaviral sequences, amplified by RT-PCR from lung tissue of 13 PUUV-seropositive Myodes regulus, were designated MUJV. The full-length S segment, a partial 208 nt region of the S segment, a full-length M segment and a 241 nt region of the Gc glycoprotein-encoding M segment were sequenced from four, eight, one and seven MUJV strains, respectively. The GenBank accession numbers for the S and M genomic sequences are provided in Table 2.
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). A hypothetical second open reading frame was identified, as for PUUV, at nt 83–355 and encoding 90 aa. Further analysis of a 208 nt region of the S genomic segment showed that MUJV differed by 18 and 26 % at the nucleotide level, respectively, from the PUUV-related TOB and CRF110 strains, amplified from Myodes rufocanus captured in Hokkaido, Japan, and Far East Russia. The interstrain variation among MUJV strains from Jeollabuk (seven strains) and Gangwon (five strains) provinces based on a 208 nt region of the S genomic segment was 16.8–19.2 % and 1.4–2.9 % at the nucleotide and amino acid levels, respectively. In the hypervariable region of the nucleocapsid protein, between aa 244 and 269, MUJV diverged by 3–5 aa from PUUV strains. However, the functional significance of these substitutions is unknown.
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). The genetic distance of MUJV and PUUV strains was 19.9–25.7 % at the nucleotide level and 8.8–11.3 % at the amino acid level.
Phylogenetic analyses of MUJV
A neighbour-joining phylogenetic tree based on the entire S segment showed that MUJV was genetically distinct from PUUV strains (Fig. 2a). Similar topologies were found in phylogenetic trees based on the entire M segment of MUJV (Fig. 2b). Phylogenetic trees based on a 208 nt region of the S segment (Fig. 2c) and a 241 nt region of the Gc glycoprotein-encoding M segment (data not shown) indicated clustering of MUJV strains by geographical origin. Within the MUJV lineage, strains from Jeollabuk and Gangwon provinces were phylogenetically distinguishable (Fig. 2c). Moreover, sublineages of MUJV were found in voles captured at Mt Deogyu and Suseongdae (Jeollabuk province) and at Mt Gyebang and Mt Gachilbong (Gangwon province).
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). Myodes regulus shared the same ancestral node as other Myodes voles but formed a different node from Microtus and Pitymys voles.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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; Vapalahti et al., 2003). Thus, by constructing phylogenetic trees based on mitochondrial or nuclear gene DNA sequences of rodents in defined subfamilies, the robust rodent–hantavirus association should allow targeted discovery of new hantaviruses. In applying this predictive paradigm to Apodemus mice, a new hantavirus from the Korean field mouse (A. peninsulae) was recently isolated (Baek et al., 2006). By extending this approach to arvicolid rodents, the royal vole (Myodes regulus) was hypothesized as harbouring a hantavirus because of its close phylogenetic proximity to bank voles (Myodes glareolus) and grey-sided voles (Myodes rufocanus), which are known reservoirs. Thus, the search for a PUUV-like hantavirus in Korea was focused on Myodes regulus as a means of ascertaining the hantavirus involved in HFRS cases occurring annually in Korea (Lee, 1982; Sachar et al., 2003), which show a higher antibody titre to PUUV than to HTNV by double-sandwich IgM ELISA.
Earlier efforts to detect hantaviruses that might account for this seroreactivity in Korea were unsuccessful. Such efforts focused largely on the reed vole (Microtus fortis) (Lee et al., 1978). In this report, royal voles from widely separated regions in Korea were found to harbour a genetically distinct hantavirus (designated MUJV). Phylogenetically intermediate between Microtus and other Myodes voles (Nowak, 1999), Myodes regulus, a member of the subfamily Arvicolinae, inhabits mountainous regions at elevations above 500 m in Korea and north-eastern China.
A. agrarius, the natural reservoir of the prototype HTNV, is the predominant species of field mouse in Korea (Baek et al., 2002; Song et al., 2000). A. peninsulae, which usually inhabits mountainous areas, is the second most common field mouse species in Korea and harbours SOOV, a genetically distinct, HFRS-causing hantavirus (Baek et al., 2006). In Scandinavia, Myodes glareolus is the primary natural reservoir of PUUV, which has also been found in Myodes rufocanus (Brummer-Korvenkontio et al., 1980; Niklasson et al., 1995; Yanagihara et al., 1984). A PUUV-related hantavirus, called Hokkaido virus, has been identified in Myodes rufocanus in Hokkaido, Japan (Kariwa et al., 1995). That Myodes regulus would harbour a hantavirus is not unexpected based on its close phylogenetic relationship with other known arvicolid rodent reservoir species. Also, that MUJV strains would share a common ancestry with PUUV and yet be evolutionarily distinct from PUUV strains is congruent with the co-evolution of these hantaviruses and their arvicolid rodent reservoir hosts.
Geographic-specific clustering has been recognized for arvicolid rodent-borne hantaviruses, including PUUV and TULV (Plyusnin et al., 1994a, b, 1995; Song et al., 2002, 2004). Recently, sequence and phylogenetic analyses of the partial M genomic segment of TULV, isolated from the European common vole (Microtus arvalis) in Poland, revealed that the genotypic segregation of Microtus-borne strains of TULV was dependent on their geographical origin (Song et al., 2004). In this study, phylogenetic trees based on the partial S and M segment sequences similarly showed geographic-specific clustering of MUJV strains from royal voles captured in Suseongdae, located 18 km north-north-west of Mt Deogyu in Jeollabuk province, as well as from royal voles captured at Mt Gachilbong, located 45 km east of Mt Gyebang, in Gangwon province.
Traditionally, the cross-PRNT has been the accepted standard for the serological classification of hantaviruses (Lee et al., 1985). The inability to isolate MUJV, despite intensive attempts over many years, is not unusual for this group of viruses, which are notoriously difficult to isolate in cell culture. In the absence of a MUJV isolate, however, sera from anti-PUUV IFA-positive Myodes regulus exhibited PRNT titres against PUUV that were two- to sixfold higher than against HTNV, SEOV or PHV. Moreover, when hantavirus isolates are unavailable, taxonomic relationships have been gleaned by using phylogenetic approaches. For example, phylogenetic analysis of partial M segment sequences has correlated well with cross-neutralization data and therefore may be a useful adjunct to classifying hantaviruses (Xiao et al., 1994). Based on the genetic divergence from PUUV and other PUUV-like hantaviruses from northern Japan, as well as the phylogenetic analyses of full-length S and M segment sequences and the PRNT data, MUJV is likely to be a new hantavirus species. However, future studies are warranted to ascertain whether MUJV causes human infection and disease.
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ACKNOWLEDGEMENTS |
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Received 3 May 2007;
accepted 8 July 2007.
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), where Myodes regulus voles were trapped during 1996–2007. Mt Deogyu (1614 m) and Suseongdae (1240 m), in Muju county, Jeollabuk province, located about 190 km south and 70 km east of Seoul, were two principal capture sites. The nine trapping sites in Gangwon province comprised Damte valley in Cheolwon county; Mt Gyebang (1577 m) in Hongcheon county; Mt Jeombong (1424 m), Mt Gachilbong (1241 m), Mt Hanseg (1104 m), Garibong (1519 m) and Hangyeryung (1307 m) in Inje county; Unduryeong (1089 m) in Pyungchang county; and Mt Whaag (1468 m) in Whacheon county. Other capture sites were Mt Myungseong (923 m), Mt Unbong (868 m), Gapyung, Pocheon and Yeonchon counties and Paju city in Gyeonggi province; Mt Gaya in Yesan county, Chungcheongnam province; Mt Joryeong (1017 m) in Munkyung county, Gyeongsangbuk province; and Yeongkwang county, Jeollanam province.
