Characterization of Imjin virus, a newly isolated hantavirus from the Ussuri white-toothed shrew (Crocidura lasiura)

Journal of Virology

Volumn 83, Issue 12, 2009, Pages 6184-6191

  Song, Jin Won ^a   Hae, Ji Kang ^a   Se, Hun Gu ^a   Sung, Sil Moon ^a   Bennett, Shannon N ^b   Song, Ki Joon ^a   Luck, Ju Baek ^a   Kim, Heung Chul ^c   O'Guinn, Monica L ^d   Chong, Sung Tae ^c   Klein, Terry A ^d   Yanagihara, Richard ^b  

^a Korea University College of Medicine   (South Korea)

^b UNIVERSITY OF HAWAII   (United States)

^c 65th Medical Brigade ^*  (United States)

^d Preventive Medicine Activity   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN G; MITOCHONDRIAL DNA; VIRUS ANTIBODY; VIRUS ANTIGEN; VIRUS RNA;

ARTICLE; CROCIDURA LASIURA; HANTAVIRUS; IMJIN VIRUS; NONHUMAN; PRIORITY JOURNAL; SHREW; VIRUS GENOME; VIRUS HEMORRHAGIC FEVER; ANIMAL; BLOOD; CERCOPITHECUS; CLASSIFICATION; FEMALE; GENETICS; ISOLATION AND PURIFICATION; KOREA; MALE; PHYLOGENY; PREVALENCE; SEASON; SERODIAGNOSIS; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE; VERO CELL; VIROLOGY; VIRUS CULTURE;

ARVICOLINAE; CROCIDURA; CROCIDURA LASIURA; CROCIDURINAE; HANTAVIRUS; MURINAE; NEOTOMINAE; RODENTIA; SIGMODONTINAE; SOREX MIRABILIS; SORICIDAE; SORICOMORPHA; SUNCUS MURINUS; THOTTAPALAYAM VIRUS; UNCLASSIFIED VIRUSES;

ANIMALS; ANTIBODIES, VIRAL; ANTIGENS, VIRAL; CERCOPITHECUS AETHIOPS; DNA, MITOCHONDRIAL; FEMALE; GENOME, VIRAL; HANTAVIRUS; KOREA; MALE; MICROSCOPY, ELECTRON, TRANSMISSION; NEUTRALIZATION TESTS; PHYLOGENY; PLAQUE ASSAY; PREVALENCE; RNA, VIRAL; SEASONS; SHREWS; VERO CELLS;

EID: 66149151721     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00371-09     Document Type: Article

References (61)

1. Arai, S., J.-W. Song, L. Sumibcay, S. N. Bennett, V. R. Nerurkar, C. Parmenter, J. A. Cook, T. L. Yates, and R. Yanagihara. 2007. Hantavirus in northern short-tailed shrew, United States. Emerg. Infect. Dis. 13:1420-1423.
2. Arai, S., S. N. Bennett, L. Sumibcay, J. A. Cook, J.-W. Song, A. Hope, C. Parmenter, V. R. Nerurkar, T. L. Yates, and R. Yanagihara. 2008. Phylogenetically distinct hantaviruses in the masked shrew (Sorex cinereus) and dusky shrew (Sorex monticolus) in the United States. Am. J. Trop. Med. Hyg. 78:348-351.
3. Arai, S., S. D. Ohdachi, M. Asakawa, H. J. Kang, G. Mocz, J. Arikawa, N. Okabe, and R. Yanagihara. 2008. Molecular phylogeny of a newfound hantavirus in the Japanese shrew mole (Urotrichus talpoides). Proc. Natl. Acad. Sci. USA 105:16296-16301.
4. Arikawa, J., A. L. Schmaljohn, J. M. Dalrymple, and C. S. Schmaljohn. 1989. Characterization of Hantaan virus envelope glycoprotein antigenic determinants defined by monoclonal antibodies. J. Gen. Virol. 70:615-624.
5. Baek, L. J., H. Kariwa, K. Lokugamage, K. Yoshimatsu, J. Arikawa, I. Takashima, J. I. Kang, S. S. Moon, S. Y. Chung, E. J. Kim, H. J. Kang, K.-J. Song, T. A. Klein, R. Yanagihara, and J.-W. Song. 2006. Soochong virus: a genetically distinct hantavirus isolated from Apodemus peninsulae in Korea. J. Med. Virol. 78:290-297.
6. Bibb, M. J., R. A. Van Etten, C. T. Wright, M. W. Walberg, and D. A. Clayton. 1981. Sequence and gene organization of mouse mitochondrial DNA. Cell 26:167-180. (Pubitemid 12244496)
7. Borucki, M. K., J. D. Boone, J. E. Rowe, M. C. Bohlman, E. A. Kuhn, R. DeBaca, and S. C. St. Jeor. 2000. Role of maternal antibody in natural infection of Peromyscus maniculatus with Sin Nombre virus. J. Virol. 74:2426-2429.
8. Botten, J., K. Mirowsky, C. Ye, K. Gottlieb, M. Saavedra, L. Ponce, and B. Hjelle. 2002. Shedding and intracage transmission of Sin Nombre hantavirus in the deer mouse (Peromyscus maniculatus) model. J. Virol. 76:7587-7594.
9. Calisher, C. H., J. J. Root, J. N. Mills, J. E. Rowe, S. A. Reeder, E. S. Jentes, K. Wagoner, and B. J. Beaty. 2005. Epizootiology of Sin Nombre and El Moro Canyon hantaviruses, southeastern Colorado, 1995-2000. J. Wildl. Dis. 41:1-11.
10. Carey, D. E., R. Reuben, K. N. Panicker, R. E. Shope, and R. M. Myers. 1971. Thottapalayam virus: a presumptive arbovirus isolated from a shrew in India. Indian J. Med. Res. 59:1758-1760.
11. Cho, H. W., and C. R. Howard. 1999. Antibody responses in humans to an inactivated hantavirus vaccine (Hantavax). Vaccine 17:2569-2575. (Pubitemid 29314450)
12. Chu, Y. K., H. W. Lee, J. W. LeDuc, C. S. Schmaljohn, and J. M. Dalrymple. 1994. Serological relationships among viruses in the Hantavirus genus, family Bunyaviridae. Virology 198:196-204.
13. Cueto, G. R., R. Cavia, C. Bellomo, P. J. Padula, and O. V. Suárez. 2008. Prevalence of hantavirus infection in wild Rattus norvegicus and R. rattus populations of Buenos Aires City, Argentina. Trop. Med. Int. Health 13:46-51.
14. Douglass, R. J., T. Wilson, W. J. Semmens, S. N. Zanto, C. W. Bond, R. C. Van Horn, and J. N. Mills. 2001. Longitudinal studies of Sin Nombre virus in deer mouse-dominated ecosystems of Montana. Am. J. Trop. Med. Hyg. 65:33-41.
15. Dubey, S., N. Salamin, S. D. Ohdachi, P. Barrière, and P. Vogel. 2007. Molecular phylogenetics of shrews (Mammalia: Soricidae) reveal timing of transcontinental colonizations. Mol. Phylogenet. Evol. 44:126-137.
16. Duchin, J. S., F. T. Koster, C. J. Peters, G. L. Simpson, B. Tempest, S. R. Zaki, T. G. Ksiazek, P. E. Rollin, S. Nichol, E. T. Umland, R. L. Moolenaar, S. E. Reef, K. B. Nolte, M. M. Gallaher, J. C. Butler, and R. F. Breiman for the Hantavirus Study Group. 1994. Hantavirus pulmonary syndrome: a clinical description of 17 patients with a newly recognized disease. N. Engl. J. Med. 330:949-955.
17. Easterbrook, J. D., M. C. Zink, and S. L. Klein. 2007. Regulatory T cells enhance persistence of the zoonotic pathogen Seoul virus in its reservoir host. Proc. Natl. Acad. Sci. USA 104:15502-15507.
18. Easterbrook, J. D., and S. L. Klein. 2008. Immunological mechanisms mediating hantavirus persistence in rodent reservoirs. PLoS Pathog. 4:e1000172.
19. Gajdusek, D. C. 1956. Hemorrhagic fevers in Asia: a problem in medical ecology. Geogr. Rev. 46:20-42.
20. Gavrilovskaya, I. N., N. S. Apekina, Y. A. Myasnikov, A. D. Bernshtein, E. V. Ryltseva, E. A. Gorbachkova, and M. P. Chumakov. 1983. Features of circulation of hemorrhagic fever with renal syndrome (HFRS) virus among small mammals in the European U.S.S.R. Arch. Virol. 75:313-316.
21. Giglioli, H. H., and T. Salvadori. 1887. Brief notes on the fauna of Corea and the adjoining coast of Manchuria. Proc. Zool. Soc. Lond. 6:580-597.
22. Glass, G. E., J. E. Childs, G. W. Korch, and J. W. LeDuc. 1988. Association of intraspecific wounding with hantaviral infection in wild rats (Rattus norvegicus). Epidemiol. Infect. 101:459-472.
23. Heiske, A., B. Anheier, J. Pilaski, V. E. Volchkov, and H. Feldmann. 1999. A new Clethrionomys-derived hantavirus from Germany: evidence for distinct genetic sublineages of Puumala viruses in Western Europe. Virus Res. 61:101-112.
24. Hinson, E. R., S. M. Shone, M. C. Zink, G. E. Glass, and S. L. Klein. 2004. Wounding: the primary mode of Seoul virus transmission among male Norway rats. Am. J. Trop. Med. Hyg. 70:310-317.
25. Hughes, A. L., and R. Friedman. 2000. Evolutionary diversification of protein- coding genes of hantaviruses. Mol. Biol. Evol. 17:1558-1568.
26. Jackson, A. P., and M. A. Charleston. 2004. A co-phylogenetic perspective of RNA-virus evolution. Mol. Biol. Evol. 21:45-57.
27. Kang, H. J., S. N. Bennett, L. Dizney, L. Sumibcay, S. Arai, L. A. Ruedas, J.-W. Song, and R. Yanagihara. Host switch during evolution of a genetically distinct hantavirus in the American shrew mole (Neurotrichus gibbsii). Virology, in press.
28. Khaiboullina, S. F., S. P. Morzunov, and S. C. St. Jeor. 2005. Hantaviruses: molecular biology, evolution and pathogenesis. Curr. Mol. Med. 5:773-790.
29. Klempa, B., E. Fichet-Calvet, E. Lecompte, B. Auste, V. Aniskin, H. Meisel, P. Barrier, L. Koivogui, J. ter Meulen, and D. H. Krüger. 2007. Novel hantavirus sequences in shrew, Guinea. Emerg. Infect. Dis. 13:520-522.
30. Kuenzi, A. J., R. J. Douglass, C. W. Bond, C. H. Calisher, and J. N. Mills. 2005. Long-term dynamics of Sin Nombre viral RNA and antibody in deer mice in Montana. J. Wildl. Dis. 41:473-481.
31. Lee, H. W., G. R. French, P.-W. Lee, L. J. Baek, K. Tsuchiya, and R. S. Foulke. 1981. Observations on natural and laboratory infection of rodents with the etiologic agent of Korean hemorrhagic fever. Am. J. Trop. Med. Hyg. 30:477-482.
32. Lee, H. W., P.-W. Lee, L. J. Baek, C. K. Song, and I. W. Seong. 1981. Intraspecific transmission of Hantaan virus, the etiologic agent of Korean hemorrhagic fever, in the rodent Apodemus agrarius. Am. J. Trop. Med. Hyg. 30:1106-1112.
33. Lee, P.-W., H. L. Amyx, R. Yanagihara, D. C. Gajdusek, D. Goldgaber, and C. J. Gibbs, Jr. 1985. Partial characterization of Prospect Hill virus isolated from meadow voles in the United States. J. Infect. Dis. 152:826-829.
34. Lee, P.-W., C. J. Gibbs, Jr., D. C. Gajdusek, and R. Yanagihara. 1985. Serotypic classification of hantaviruses by indirect immunofluorescent antibody and plaque reduction neutralization tests. J. Clin. Microbiol. 22:940-944.
35. McIntyre, N. E., Y. K. Chu, R. D. Owen, A. Abuzeineh, N. De la Sancha, C. W. Dick, T. Holsomback, R. A. Nisbett, and C. Jonsson. 2005. A longitudinal study of Bayou virus, hosts, and habitat. Am. J. Trop. Med. Hyg. 73:1043-1049.
36. Nichol, S. T., C. F. Spiropoulou, S. Morzunov, P. E. Rollin, T. G. Ksiazek, H. Feldmann, A. Sanchez, J. Childs, S. Zaki, and C. J. Peters. 1993. Genetic identification of a hantavirus associated with an outbreak of acute respiratory illness. Science 262:914-917. (Pubitemid 24014083)
37. Ohdachi, S. D., M. A. Iwasa, V. A. Nesterenko, H. Abe, R. Masuda, and W. Haberl. 2004. Molecular phylogenetics of Crocidura shrews (Insectivora) in east and central Asia. J. Mammal. 85:396-403. (Pubitemid 38708768)
38. Okumura, M., K. Yoshimatsu, S. Kumperasart, I. Nakamura, M. Ogino, M. Taruishi, A. Sungdee, S. Pattamadilok, I. N. Ibrahim, S. Erlina, T. Agui, R. Yanagihara, and J. Arikawa. 2007. Development of serological assays for Thottapalayam virus, an insectivore-borne hantavirus. Clin. Vaccine Immunol. 14:173-181.
39. Plyusnin, A., O. Vapalahti, and A. Vaheri. 1996. Hantaviruses: genome structure, expression and evolution. J. Gen. Virol. 77:2677-2687.
40. Posada, D., and K. A. Crandall. 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817-818. (Pubitemid 28552116)
41. Schmaljohn, C. S., S. E. Hasty, J. M. Dalrymple, J. W. LeDuc, H. W. Lee, C. H. von Bonsdorff, M. Brummer-Korvenkontio, A. Vaheri, T. F. Tsai, H. L. Regnery, D. Goldgaber, and P.-W. Lee. 1985. Antigenic and genetic properties of viruses linked to hemorrhagic fever with renal syndrome. Science 227:1041-1044. (Pubitemid 15142044)
42. Schmidt, H. A., K. Strimmer, M. Vingron, and A. von Haeseler. 2002. TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18:502-504. (Pubitemid 34284960)
43. Smith, M. F., and J. L. Patton. 1991. Variation in mitochondrial cytochrome b sequence in natural populations of South American akodontine rodents (Muridae: Sigmodontinae). Mol. Biol. Evol. 8:85-103.
44. Song, J.-W., L. J. Baek, C. S. Schmaljohn, and R. Yanagihara. 2007. Thottapalayam virus: a prototype shrew-borne hantavirus. Emerg. Infect. Dis. 13:980-985.
45. Song, J.-W., S. H. Gu, S. N. Bennett, S. Arai, M. Puorger, M. Hilbe, and R. Yanagihara. 2007. Seewis virus, a genetically distinct hantavirus in the Eurasian common shrew (Sorex araneus). Virol. J. 4:114.
46. Song, J.-W., H. J. Kang, K. J. Song, T. T. Truong, S. N. Bennett, S. Arai, N. U. Truong, and R. Yanagihara. 2007. Newfound hantavirus in Chinese mole shrew, Vietnam. Emerg. Infect. Dis. 13:1784-1787.
47. Song, K.-J., L. J. Baek, S. S. Moon, S. J. Ha, S. H. Kim, K. S. Park, T. A. Klein, W. Sames, H.-C. Kim, J. S. Lee, R. Yanagihara, and J.-W. Song. 2007. Muju virus, a newfound hantavirus harbored by the arvicolid rodent Myodes regulus in Korea. J. Gen. Virol. 88:3121-3129.
48. Spurr, A. R. 1969. A low-viscosity epoxy resin embedding medium for electron microscopy. J. Ultrastruct. Res. 26:31-43.
49. Stamatakis, A., P. Hoover, and J. Rougemont. 2008. A rapid bootstrap algorithm for the RAxML web-servers. Syst. Biol. 75:758-771.
50. Swofford, D. L. 2003. PAUP* version 4: phylogenetic analysis using parsimony (*and other methods). Sinauer Associates, Sunderland, MA.
51. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680. (Pubitemid 24354800)
52. Tkachenko, E. A., A. P. Ivanov, M. A. Donets, Y. A. Miasnikov, E. V. Ryltseva, L. K. Gaponova, V. N. Bashkirtsev, N. M. Okulova, S. G. Drozdov, R. A. Slonova, G. P. Somov, and T. I. Astakhova. 1983. Potential reservoir and vectors of haemorrhagic fever with renal syndrome (HFRS) in the U.S.S.R. Ann. Soc. Belg. Med. Trop. 63:267-269.
53. Trencseni, T., and B. Keleti. 1971. Clinical aspects and epidemiology of haemorrhagic fever with renal syndrome. Analysis of clinical and epidemiological experiences in Hungary. Akademiai Kiado, Budapest, Hungary.
54. Vapalahti, O., J. Mustonen, A. Lundkvist, H. Henttonen, A. Plyusnin, and A. Vaheri. 2003. Hantavirus infections in Europe. Lancet Infect. Dis. 3:653-661.
55. Xiao, S.-Y., J. W. LeDuc, Y. K. Chu, and C. S. Schmaljohn. 1994. Phylogenetic analyses of virus isolates in the genus Hantavirus, family Bunyaviridae. Virology 198:205-217.
56. Yadav, P. D., M. J. Vincent, and S. T. Nichol. 2007. Thottapalayam virus is genetically distant to the rodent-borne hantaviruses, consistent with its isolation from the Asian house shrew (Suncus murinus). Virol. J. 4:80.
57. Yanagihara, R. 1990. Hantavirus infection in the United States: epizootiology and epidemiology. Rev. Infect. Dis. 12:449-457.
58. Yanagihara, R., D. Goldgaber, P.-W. Lee, H. L. Amyx, D. C. Gajdusek, C. J. Gibbs, Jr., and A. Svedmyr. 1984. Propagation of nephropathia epidemica virus in cell culture. Lancet i:1013. (Pubitemid 14148910)
59. Yanagihara, R., H. L. Amyx, and D. C. Gajdusek. 1985. Experimental infection with Puumala virus, the etiologic agent of nephropathia epidemica, in bank voles (Clethrionomys glareolus). J. Virol. 55:34-38.
60. Yanagihara, R., and D. C. Gajdusek. 1988. Hemorrhagic fever with renal syndrome: a historical perspective and review of recent advances, p. 151-188. In J. H. S. Gear (ed.), CRC handbook of viral and rickettsial hemorrhagic fevers. CRC Press, Inc., Boca Raton, FL.
61. Zeller, H. G., N. Karabatsos, C. H. Calisher, J. P. Digoutte, C. B. Cropp, F. A. Murphy, and R. E. Shope. 1989. Electron microscopic and antigenic studies of uncharacterized viruses. II. Evidence suggesting the placement of viruses in the family Bunyaviridae. Arch. Virol. 108:211-227. (Pubitemid 20046968)