Open Access

Genetic diversity and phylogeography of Seewis virus in the Eurasian common shrew in Finland and Hungary

  • Hae Ji Kang1,
  • Satoru Arai2,
  • Andrew G Hope3,
  • Jin-Won Song4,
  • Joseph A Cook3 and
  • Richard Yanagihara1Email author
Virology Journal20096:208

DOI: 10.1186/1743-422X-6-208

Received: 07 September 2009

Accepted: 24 November 2009

Published: 24 November 2009

Abstract

Recent identification of a newfound hantavirus, designated Seewis virus (SWSV), in the Eurasian common shrew (Sorex araneus), captured in Switzerland, corroborates decades-old reports of hantaviral antigens in this shrew species from Russia. To ascertain the spatial or geographic variation of SWSV, archival liver tissues from 88 Eurasian common shrews, trapped in Finland in 1982 and in Hungary during 1997, 1999 and 2000, were analyzed for hantavirus RNAs by reverse transcription-polymerase chain reaction. SWSV RNAs were detected in 12 of 22 (54.5%) and 13 of 66 (19.7%) Eurasian common shrews from Finland and Hungary, respectively. Phylogenetic analyses of S- and L-segment sequences of SWSV strains, using maximum likelihood and Bayesian methods, revealed geographic-specific genetic variation, similar to the phylogeography of rodent-borne hantaviruses, suggesting long-standing hantavirus-host co-evolutionary adaptation.

Findings

A paradigm-altering chapter in hantavirology is unfolding with the discovery of genetically distinct hantaviruses in multiple species of shrews (Order Soricomorpha, Family Soricidae), including the northern short-tailed shrew (Blarina brevicauda) [1], Chinese mole shrew (Anourosorex squamipes) [2], masked shrew (Sorex cinereus) [3], dusky shrew (Sorex monticolus) [3], Therese's shrew (Crocidura theresae) [4] and Ussuri white-toothed shrew (Crocidura lasiura) [5]. Also, whole-genome analysis of Thottapalayam virus (TPMV), a hantavirus isolated from the Asian house shrew (Suncus murinus) [6, 7], demonstrates a separate phylogenetic clade, consistent with an early evolutionary divergence from rodent-borne hantaviruses [8, 9]. Moreover, recent identification of hantaviruses in moles (Family Talpidae) further challenges the conventional view that rodents are the primordial reservoir hosts of hantaviruses, and suggests that their evolutionary origins and zoogeographic history are far more ancient and complex than formerly conjectured [1012].

Previous analysis of the full-length S and partial M and L segments of a newfound hantavirus, designated Seewis virus (SWSV), detected in the Eurasian common shrew (Sorex araneus), captured in the Swiss canton of Graubünden [13], corroborates earlier reports of hantaviral antigens in this shrew species from Russia, Belgium and the former Yugoslavia [1416]. As its name implies, the Eurasian common shrew (Subfamily Soricinae) is among the most widely dispersed small mammal species in Eurasia. Its vast geographic range, which extends throughout Northern Europe, including Scandinavia and Great Britain (but excluding Ireland), and across Russia (Fig. 1), provided an opportunity to investigate the genetic diversity and phylogeography of SWSV.
https://static-content.springer.com/image/art%3A10.1186%2F1743-422X-6-208/MediaObjects/12985_2009_Article_722_Fig1_HTML.jpg
Figure 1

Maps with shaded areas, showing the (A) geographic range of the Eurasian common shrew ( Sorex araneus ) and administrative districts in (B) Hungary and (C) Finland, where trapping was conducted.

Archival liver tissues from 88 Eurasian common shrews, trapped in Finland in 1982 and in Hungary during 1997, 1999 and 2000 (Table 1 and Fig. 1), were retrieved from deep-freeze storage at the Museum of Southwestern Biology, of the University of New Mexico. Total RNA was extracted using the PureLink Micro-to-Midi total RNA purification kit (Invitrogen, San Diego, CA), and cDNA was synthesized using SuperScript III First-Strand Synthesis System (Invitrogen) and an oligonucleotide primer (OSM55: 5'-TAGTAGTAGACTCC-3'), designed from the genus-specific conserved 3'-end of the S, M and L segments of all hantaviruses. For reverse transcription-polymerase chain reaction (RT-PCR), primers, based on highly conserved regions of shrew-borne hantavirus genomes, were employed: S (outer: 5'-TAGTAGTAGACTCC-3', 5'-AGCTCNGGATCCATNTCATC-3'; inner: 5'-AGYCCNGTNATGRGWGTNRTYGG-3', 5'-ANGAYTGRTARAANGANGAYTTYTT-3'); and L (outer: 5'-ATGAARNTNTGTGCNATNTTTGA-3', 5'-GCNGARTTRTCNCCNGGNGACCA-3'; inner: 5'-ATNWGHYTDAARGGNATGTCNGG-3', 5'-CCNGGNGACCAYTTNGTDGCATC-3'). Nested PCR cycling conditions and methods for DNA sequencing have been previously described [3, 11, 12].
Table 1

RT-PCR detection of SWSV RNA in Eurasian common shrews.

Country

Administrative

District

Sampling

Year

Number Tested

Number Positive

Finland

Etelä-Suomen Lääni

1982

10

4

 

Lappi

1982

3

1

 

Oulun Lääni

1982

9

7

Hungary

Györ-Sopron-Moson

1997

18

10

 

Zala

1999, 2000

48

3

SWSV RNAs were detected by RT-PCR in 12 of 22 (54.5%) and 13 of 66 (19.7%) Eurasian common shrews from Finland and Hungary, respectively (Table 1). Prevalence of SWSV infection was as high as 77.8% (7 of 9) in Oulun Lääni, Finland, and as low as 6.3% (3 of 48) in Zala, Hungary. Analysis of the partial S- and L-genomic sequences of SWSV showed considerable divergence from the SWSV prototype mp70 strain at the nucleotide level (Table 2): S, 11.9-19.4%; and L, 18.1-21.8%. However, the S- and L-segment nucleotide sequence variation of SWSV strains within a specific geographic region was low, ranging from 0-0.7% and 0-1.0% in Etelä-Suomen, 0.3-1.3% and 0-6.0% in Oulun Lääni, 0.2-4.9% and 0-4.6% in Györ-Sopron-Moson, and 0.2% and 0-2.6% in Zala. Moreover, there was strong conservation of the encoded proteins with ≤ 3.1% variation at the amino acid level among SWSV strains from Finland, Hungary and Switzerland.
Table 2

Sequence similarities (%) of the partial S and L segments of SWSV mp70 and SWSV strains from Sorex araneus sampled in Finland and Hungary.

   

S segment

L segment

Country

District

SWSV strain

(nt)*

(aa)*

400 nt

133 aa

Finland

Etelä-Suomen Lääni

DGR18226

85.7 (928)

99.4 (308)

81.3

98.8

  

DGR18228

87.1 (616)

98.0 (204)

81.7

99.3

  

DGR18279

86.9 (616)

97.5 (204)

81.5

99.3

  

DGR18283

88.1 (328)

100 (108)

81.9

99.3

 

Lappi

DGR18207

81.5 (394)

93.9 (131)

80.1

97.8

 

Oulun Lääni

DGR18874

84.4 (394)

98.5 (131)

79.1

97.1

  

DGR18887

85.8 (616)

98.5 (204)

80.0

99.3

  

DGR18888

-

-

80.2

99.3

  

DGR18889

85.7 (612)

98.0 (203)

78.9

98.5

  

DGR18890

80.6 (250)

80.7 (83)

79.5

99.2

  

DGR18891

85.8 (616)

98.5 (204)

79.3

98.4

  

DGR18893

-

-

80.4

99.3

Hungary

Györ-Sopron-Moson

MSB95458

86.0 (336)

97.3 (111)

80.5

100.0

  

MSB95461

86.2 (327)

100 (108)

79.9

99.3

  

MSB95462

86.9 (639)

99.1 (212)

80.1

99.3

  

MSB95463

87.2 (1146)

99.5 (381)

79.5

100.0

  

MSB95464

86.4 (720)

98.2 (239)

80.5

100.0

  

MSB95467

-

-

78.2

98.6

  

MSB95468

87.2 (660)

99.5 (219)

78.9

100.0

  

MSB95471

-

-

80.1

100.0

  

MSB95475

-

-

80.6

100.0

  

MSB95480

85.6 (928)

99.4 (308)

79.5

99.3

 

Zala

MSB94609

85.2 (639)

97.2 (211)

80.9

97.0

  

MSB94615

85.7 (616)

97.7 (204)

81.1

99.3

  

MSB95322

-

-

81.3

99.3

Abbreviations: SWSV, Seewis virus. nt, nucleotides; aa, amino acids.

*Percent similarities for the S segment are shown for varying lengths of nucleotides and amino acids (shown in parentheses), whereas for the L segment, similarities are shown for 400 nucleotides and 133 amino acids.

An exception was the partial S-segment sequence of SWSV strain DGR18890 from Oulun Lääni, which was highly incongruent, showing marked divergence of nearly 20% at the nucleotide and amino acid levels (Table 2). Analysis, using multiple recombination-detection methods, including GENECONV, Bootscan, Chimaera, 3SEQ, RDP, SiScan, MaxChi and HyPhy Single Recombinant Breakpoint [17], failed to disclose any evidence of recombination. However, analyses of full-length genomic sequences of SWSV strains would be required to demonstrate intra-lineage recombination events. Apart from the above-mentioned incongruity, the inability to amplify the S segment in six of the 25 L-segment RT-PCR positive tissues, despite repeated attempts using numerous primers, may be the result of low viral titers or inadequate sensitivity of the PCR primers. Intensive efforts are ongoing to resolve this important issue.

Phylogenetic analyses of the 250-nucleotide S- and 400-nucleotide L-segment sequences, generated using maximum-likelihood and Bayesian methods, implemented in PAUP* (Phylogenetic Analysis Using Parsimony, 4.0b10) [18], RAxML Blackbox web-server [19] and MrBayes 3.1 [20], under the best-fit GTR+I+Γ model of evolution using jModeltest 0.1.1 [21], showed geographic-specific clustering of SWSV strains (Fig. 2), similar to the phylogeographic variation demonstrated previously for rodent-borne hantaviruses, including Hantaan virus in the striped field mouse (Apodemus agrarius) [22], Soochong virus in the Korean field mouse (Apodemus peninsulae) [23], Puumala virus in the bank vole (Myodes glareolus) [2427], Muju virus in the royal vole (Myodes regulus) [28], Tula virus in the European common vole (Microtus arvalis) [29] and Andes virus in the long-tailed colilargo (Oligoryzomys longicaudatus) [30]. Identical topologies resulted from analysis of longer S-segment sequences of SWSV strains (Table 2).
https://static-content.springer.com/image/art%3A10.1186%2F1743-422X-6-208/MediaObjects/12985_2009_Article_722_Fig2_HTML.jpg
Figure 2

Phylogenetic tree generated by the Bayesian method, under the best-fit GTR+I+Γ model of evolution, based on the L-genomic segment of SWSV and other well-characterized hantaviruses. The phylogenetic positions of SWSV variants from Finland and Hungary are shown in relationship to SWS (Seewis) mp70 (EF636026) from the Eurasian common shrew (Sorex araneus), ARR (Ash River) MSB73418 (EF619961) from the masked shrew (Sorex cinereus), JMS (Jemez Springs) MSB144475 (FJ593501) from the dusky shrew (Sorex monticolus), CBN (Cao Bang) CBN-3 (EF543525) from the Chinese mole shrew (Anourosorex squamipes), RPL (Camp Ripley) MSB89863 (EF540771) from the northern short-tailed shrew (Blarina brevicauda), TPM (Thottapalayam) VRC66412 (EU001330) from the Asian house shrew (Suncus murinus), MJN (Imjin) Cl05-11 (EF641806) from the Ussuri white-toothed shrew (Crocidura lasiura), ASA (Asama) N10 (EU929078) from the Japanese shrew mole (Urotrichus talpoides), OXB (Oxbow) Ng1453 (FJ593497) from the American shrew mole (Neurotrichus gibbsii), and NVA (Nova) MSB95703 (FJ593498) from the European common mole (Talpa europaea). Also shown are representative rodent-borne hantaviruses, including HTN (Hantaan) 76-118 (NC_005222), SOO (Soochong) SOO-1 (DQ056292), DOB (Dobrava) Greece (NC_005235), SEO (Seoul) 80-39 (NC_005238), TUL (Tula) 5302v (NC_005226), PUU (Puumala) Sotkamo (NC_005225), PH (Prospect Hill) PH-1 (EF646763), SN (Sin Nombre) NMH10 (NC_005217), and AND (Andes) Chile9717869 (NC_003468). GenBank accession numbers for the L-segment sequences of SWSV strains are GQ293099, GQ293100, GQ293101, GQ293102, GQ293103, GQ293108, GQ293109, GQ293110, GQ293111, GQ293112, GQ293113, GQ293114 for Finland; and GQ293097, GQ293098, GQ293106, GQ293107, GQ293115, GQ293116, GQ293117, GQ293118, GQ293119, GQ293120, GQ293121, GQ293122, GQ293123 for Hungary. For the S-segment sequences of SWSV strains, GenBank accession numbers were GU186445, GQ293125, GU186444, GQ293126, GQ293129, GQ293130, GQ293131, GQ293132, GQ293133, GQ293134 for Finland; and GQ293124, GU186442, GQ293127, GQ293128, GU186443, GQ293135, GQ293136, GQ293137, GQ293138 for Hungary. The numbers at each node are posterior node probabilities based on 30,000 trees: two replicate Markov Chain Monte Carlo runs consisting of four chains of two million generations each sampled every 100 generations with a burn-in of 5,000 (25%). The scale bar indicates nucleotide substitutions per site.

Because shrews are inherently difficult to identify by morphological features alone, host verification of SWSV-infected shrews was confirmed by analyzing voucher specimens and sequencing the entire 1,140-base pair cytochrome b gene of mitochondrial DNA (mtDNA), amplified by PCR, using previously described universal primers (5'-CGAAGCTTGATATGAAAAACCATCGTTG-3' and 5'-GCAGCCCCTCAGAATGATATTTGTCCAC-3'). mtDNA sequences were deposited into GenBank (GQ374412-GQ374437), and the identities of the 25 hantavirus-infected hosts were assessed using a Bayesian approach (5 million generation with burn-in of 5000 discarded) that was mid-point rooted (tree not shown). All SWSV-infected shrews were confirmed as Sorex araneus. However, the Eurasian common shrew exhibits significant chromosomal polymorphism throughout its geographic range [31]. Previous studies suggest that several chromosomal races of Eurasian common shrews are present in Finland and Hungary. Whether or not the sub-lineages of SWSV can be traced to potentially distinct evolutionary histories of these races is a matter of conjecture and requires future investigation.

Because the original report of SWSV was based on a single Eurasian common shrew from Switzerland [13], there has been understandable reluctance in fully accepting this hantavirus-soricid association. Data from the present study, however, provide compelling evidence that this soricine shrew species harbors SWSV across its broad geographic range. As further support, in a separate study, Sorex araneus, as well as the tundra shrew (Sorex tundrensis) and Siberian large-toothed shrew (Sorex daphaenodon), have been shown to harbor genetic variants of SWSV in six widely separated administrative regions of Western and Eastern Siberia [32]. Similarly, the American water shrew (Sorex palustris), Trowbridge's shrew (Sorex trowbridgii) and vagrant shrew (Sorex vagrans) in North America harbor genetic variants of Jemez Springs virus (H.J. Kang and R. Yanagihara, unpublished), which was originally found in the dusky shrew [3]. When viewed within this context, the demonstration of SWSV in Eurasian common shrews from Finland and Hungary lends support to the hypothesis that common ancestral hantaviruses established themselves in ancestors of present-day soricine shrew species, with subsequent cross-species transmission and local host-specific adaptation.

As noted, SWSV RNAs were found in Eurasian common shrews captured in Finland more than 25 years ago. Analysis of hantavirus sequences amplified from tissues of Eurasian common shrews and other soricine shrew species more recently trapped in these same sites in Finland would be extremely valuable, in providing insights into the evolutionary rate of SWSV. Such studies are now underway.

The emerging story of previously unrecognized hantaviruses in soricomorphs has been greatly accelerated by the availability of an extensive, meticulously curated, small-mammal frozen-tissue collection, housed at the Museum of Southwestern Biology. That is, while these tissues were not collected for the purposes of our current and past studies, their ready accessibility has facilitated the rapid acquisition of new knowledge about the spatial distribution of hantaviruses in nonrodent reservoir hosts [2, 3, 12]. As such, these opportunistic studies provide convincing justification and strong testament for the establishment and long-term maintenance of these repositories for future scientific inquiry. Additional hantaviruses and other zoonotic agents are likely to be successfully mined from such banked tissues, by employing powerful microarray and ultra high-throughput sequencing technologies.

Declarations

Acknowledgements

Dr. Duane A. Schlitter and Dr. Gabor R. Racz collected the shrew tissues in Finland and Hungary, respectively. Ms. Laarni Sumibcay provided technical assistance. This work was supported in part by U.S. Public Health Service grants R01AI075057 from the National Institute of Allergy and Infectious Diseases, and P20RR018727 (Centers of Biomedical Research Excellence) and G12RR003061 (Research Centers in Minority Institutions) from the National Center for Research Resources, National Institutes of Health.

Authors’ Affiliations

(1)
Departments of Pediatrics and of Tropical Medicine, Medical Microbiology and Pharmacology, John A. Burns School of Medicine, University of Hawaii at Manoa
(2)
Infectious Disease Surveillance Center, National Institute of Infectious Diseases
(3)
Department of Biology and Museum of Southwestern Biology, University of New Mexico
(4)
Department of Microbiology, College of Medicine, and Institute for Viral Diseases, Korea University

References

  1. Arai S, Song J-W, Sumibcay L, Bennett SN, Nerurkar VR, Parmenter C, Cook JA, Yates TL, Yanagihara R: Hantavirus in northern short-tailed shrew, United States. Emerg Infect Dis 2007, 13: 1420-1423.PubMed CentralView ArticlePubMedGoogle Scholar
  2. Song J-W, Kang HJ, Song KJ, Truong TT, Bennett SN, Arai S, Truong NU, Yanagihara R: Newfound hantavirus in Chinese mole shrew, Vietnam. Emerg Infect Dis 2007, 13: 1784-1787.PubMed CentralView ArticlePubMedGoogle Scholar
  3. Arai S, Bennett SN, Sumibcay L, Cook JA, Song J-W, Hope A, Parmenter C, Nerurkar VR, Yates TL, Yanagihara R: Phylogenetically distinct hantaviruses in the masked shrew ( Sorex cinereus ) and dusky shrew ( Sorex monticolus ) in the United States. Am J Trop Med Hyg 2008, 78: 348-351.PubMed CentralPubMedGoogle Scholar
  4. Klempa B, Fichet-Calvet E, Lecompte E, Auste B, Aniskin V, Meisel H, Barriere P, Koivogui L, ter Meulen J, Kruger DH: Novel hantavirus sequences in shrew, Guinea. Emerg Infect Dis 2007, 13: 520-522. 10.3201/eid1303.061198PubMed CentralView ArticlePubMedGoogle Scholar
  5. Song J-W, Kang HJ, Gu SH, Moon SS, Bennett SN, Song KJ, Baek LJ, Kim HC, O'Guinn ML, Chong ST, Klein TA, Yanagihara R: Characterization of Imjin virus, a newly isolated hantavirus from the Ussuri white-toothed shrew ( Crocidura lasiura ). J Virol 2009, 83: 6184-6191. 10.1128/JVI.00371-09PubMed CentralView ArticlePubMedGoogle Scholar
  6. Carey DE, Reuben R, Panicker KN, Shope RE, Myers RM: Thottapalayam virus: A presumptive arbovirus isolated from a shrew in India. Indian J Med Res 1971, 59: 1758-1760.PubMedGoogle Scholar
  7. Zeller HG, Karabatsos N, Calisher CH, Digoutte J-P, Cropp CB, Murphy FA, Shope RE: Electron microscopic and antigenic studies of uncharacterized viruses. II. Evidence suggesting the placement of viruses in the family Bunyaviridae . Arch Virol 1989, 108: 211-227. 10.1007/BF01310935View ArticlePubMedGoogle Scholar
  8. Song J-W, Baek LJ, Schmaljohn CS, Yanagihara R: Thottapalayam virus, a prototype shrewborne hantavirus. Emerg Infect Dis 2007, 13: 980-985.PubMed CentralView ArticlePubMedGoogle Scholar
  9. Yadav PD, Vincent MJ, Nichol ST: Thottapalayam virus is genetically distant to the rodent-borne hantaviruses, consistent with its isolation from the Asian house shrew ( Suncus murinus ). Virol J 2007, 4: 80. 10.1186/1743-422X-4-80PubMed CentralView ArticlePubMedGoogle Scholar
  10. Arai S, Ohdachi SD, Asakawa M, Kang HJ, Mocz G, Arikawa J, Okabe N, Yanagihara R: Molecular phylogeny of a newfound hantavirus in the Japanese shrew mole ( Urotrichus talpoides ). Proc Natl Acad Sci USA 2008, 105: 16296-16301. 10.1073/pnas.0808942105PubMed CentralView ArticlePubMedGoogle Scholar
  11. Kang HJ, Bennett SN, Dizney L, Sumibcay L, Arai S, Ruedas LA, Song J-W, Yanagihara R: Host switch during evolution of a genetically distinct hantavirus in the American shrew mole ( Neurotrichus gibbsii ). Virology 2009, 388: 8-14. 10.1016/j.virol.2009.03.019PubMed CentralView ArticlePubMedGoogle Scholar
  12. Kang HJ, Bennett SN, Sumibcay L, Arai S, Hope AG, Mocz G, Song J-W, Cook JA, Yanagihara R: Evolutionary insights from a genetically divergent hantavirus harbored by the European common mole ( Talpa europaea ). PLoS One 2009, 4: e6149. 10.1371/journal.pone.0006149PubMed CentralView ArticlePubMedGoogle Scholar
  13. Song JW, Gu SH, Bennett SN, Arai S, Puorger M, Hilbe M, Yanagihara R: Seewis virus, a genetically distinct hantavirus in the Eurasian common shrew ( Sorex araneus ). Virol J 2007, 4: 114. 10.1186/1743-422X-4-114PubMed CentralView ArticlePubMedGoogle Scholar
  14. Tkachenko EA, Ivanov AP, Donets MA, Miasnikov YA, Ryltseva EV, Gaponova LK, Bashkirtsev VN, Okulova NM, Drozdov SG, Slonova RA, Somov GP: Potential reservoir and vectors of haemorrhagic fever with renal syndrome (HFRS) in the U.S.S.R. Ann Soc Belg Med Trop 1983, 63: 267-269.PubMedGoogle Scholar
  15. Clement J, McKenna P, Leirs H, Verhagen R, Lefevre A, Song G, Tkachenko E, Groen G: Hantavirus infections in rodents. In Virus Infections of Rodents and Lagomorphs. Edited by: Osterhaus ADME. Amsterdam: Elsevier Science BV; 1994:295-316.Google Scholar
  16. Gligic A, Stojanovic R, Obradovic M, Hlaca D, Dimkovic N, Diglisic G, Lukac V, Ler Z, Bogdanovic R, Antonijevic B, Ropac D, Avsic T, LeDuc JW, Ksiazek T, Yanagihara R, Gajdusek DC: Hemorrhagic fever with renal syndrome in Yugoslavia: Epidemiologic and epizootiologic features of a nationwide outbreak in 1989. Eur J Epidemiol 1992, 8: 816-825. 10.1007/BF00145326View ArticlePubMedGoogle Scholar
  17. Pond SL, Frost SDW, Muse SV: HyPhy: hypothesis testing using phylogenies. Bioinformatics 2005, 21: 676-679. 10.1093/bioinformatics/bti079View ArticlePubMedGoogle Scholar
  18. Swofford DL: PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sinauer Associates, Sunderland, Massachusetts; 2003.Google Scholar
  19. Stamatakis A, Hoover P, Rougemont J: A rapid bootstrap algorithm for the RAxML web servers. Syst Biol 2008, 57: 758-771. 10.1080/10635150802429642View ArticlePubMedGoogle Scholar
  20. Ronquist F, Huelsenbeck JP: MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19: 1572-1574. 10.1093/bioinformatics/btg180View ArticlePubMedGoogle Scholar
  21. Posada D: jModelTest: Phylogenetic Model Averaging. Mol Biol Evol 2008, 25: 1253-1256. 10.1093/molbev/msn083View ArticlePubMedGoogle Scholar
  22. Song J-W, Baek LJ, Kim SH, Kho EY, Kim JH, Yanagihara R, Song K-J: Genetic diversity of Apodemus agrarius -borne Hantaan virus in Korea. Virus Genes 2000, 21: 227-232. 10.1023/A:1008199800011View ArticlePubMedGoogle Scholar
  23. Baek LJ, Kariwa H, Lokugamage K, Yoshimatsu K, Arikawa J, Takashima I, Kang JI, Moon SS, Chung SY, Kim EJ, Kang HJ, Song K-J, Klein TA, Yanagihara R, Song J-W: Soochong virus: A genetically distinct hantavirus isolated from Apodemus peninsulae in Korea. J Med Virol 2006, 78: 290-297. 10.1002/jmv.20538View ArticlePubMedGoogle Scholar
  24. Plyusnin A, Vapalahti O, Ulfves K, Lehvaslaiho H, Apekina N, Gavrilovskaya I, Blinov V, Vaheri A: Sequences of wild Puumala virus genes show a correlation of genetic variation with geographic origin of the strains. J Gen Virol 1994, 75: 405-409. 10.1099/0022-1317-75-2-405View ArticlePubMedGoogle Scholar
  25. Plyusnin A, Vapalahti O, Lehvaslaiho H, Apekina N, Mikhailova T, Gavrilovskaya I, Laakkonen J, Niemimaa J, Henttonen H, Brummer-Korvenkontio M, Vaheri A: Genetic variation of wild Puumala viruses within the serotype, local rodent populations and individual animal. Virus Res 1995, 38: 25-41. 10.1016/0168-1702(95)00038-RView ArticlePubMedGoogle Scholar
  26. Plyusnina A, Ferenczi E, Rácz GR, Nemirov K, Lundkvist A, Vaheri A, Vapalahti O, Plyusnin A: Co-circulation of three pathogenic hantaviruses: Puumala, Dobrava, and Saaremaa in Hungary. J Med Virol 2009, 81: 2045-2052. 10.1002/jmv.21635View ArticlePubMedGoogle Scholar
  27. Garanina SB, Platonov AE, Zhuravlev VI, Murashkina AN, Yakimenko VV, Korneev AG, Shipulin GA: Genetic diversity and geographic distribution of hantaviruses in Russia. Zoonoses Public Health 2009, in press.Google Scholar
  28. Song K-J, Baek LJ, Moon SS, Ha SJ, Kim SH, Park KS, Klein TA, Sames W, Kim H-C, Lee JS, Yanagihara R, Song J-W: Muju virus, a newfound hantavirus harbored by the arvicolid rodent Myodes regulus in Korea. J Gen Virol 2007, 88: 3121-3129. 10.1099/vir.0.83139-0PubMed CentralView ArticlePubMedGoogle Scholar
  29. Song JW, Baek LJ, Song KJ, Skrok A, Markowski J, Bratosiewicz J, Kordek R, Liberski PP, Yanagihara R: Characterization of Tula virus from common voles ( Microtus arvalis ) in Poland: Evidence for geographic-specific phylogenetic clustering. Virus Genes 2004, 29: 239-247. 10.1023/B:VIRU.0000036384.50102.cfView ArticlePubMedGoogle Scholar
  30. Medina RA, Torres-Perez F, Galeno H, Navarrete M, Vial PA, Palma RE, Ferres M, Cook JA, Hjelle B: Ecology, genetic diversity and phylogeographic structure of Andes virus in humans and rodents in Chile. J Virol 2009, 83: 2446-2459. 10.1128/JVI.01057-08PubMed CentralView ArticlePubMedGoogle Scholar
  31. Searle JB, Wójcik JM: Chromosomal evolution: The case of Sorex araneus . In Evolution of Shrews. Edited by: Wójcik JM, Wolsan M. Bialowieza, Poland: Mammal Research Institute, Polish Academy of Sciences; 1998:219-268.Google Scholar
  32. Yashina L, Abramov S, Gutorov V, Dupal T, Krivopalov A, Panov V, Danchinova G, Vinogradov V, Luchnikova E, Hay J, Kang HJ, Yanagihara R: Seewis virus: Phylogeography of a shrew-borne hantavirus in Siberia, Russia. Vector-Borne Zoonotic Dis 2009, in press.Google Scholar

Copyright

© Kang et al; licensee BioMed Central Ltd. 2009

This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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