Evolutionary insights from a genetically divergent hantavirus harbored by the European common mole (Talpa europaea)

PLoS ONE

Volumn 4, Issue 7, 2009, Pages

  Kang, Hae Ji ^a,b   Bennett, Shannon N ^a   Sumibcay, Laarni ^a   Arai, Satoru ^c   Hope, Andrew G ^d   Mocz, Gabor ^e   Song, Jin Won ^b   Cook, Joseph A ^d   Yanagihara, Richard ^a  

^a UNIVERSITY OF HAWAII   (United States)

^b Korea University College of Medicine   (South Korea)

^c NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^d UNIVERSITY OF NEW MEXICO   (United States)

^e UNIVERSITY OF HAWAII   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LARGE SUBUNIT RIBOSOMAL RNA; NUCLEOCAPSID PROTEIN; SMALL SUBUNIT RIBOSOMAL RNA; PRIMER DNA; VIRUS PROTEIN;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL TISSUE; ARTICLE; BAYES THEOREM; CONTROLLED STUDY; GENETIC ANALYSIS; GENETIC VARIABILITY; GEOGRAPHICAL VARIATION (SPECIES); HANTAVIRUS; MOLE RAT; MOLECULAR EVOLUTION; NONHUMAN; NOVA VIRUS; NUCLEOTIDE SEQUENCE; PHYLOGENETIC TREE; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN SECONDARY STRUCTURE; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; SHREW; SPECIES COMPARISON; UNINDEXED SEQUENCE; VIRUS CELL INTERACTION; ANIMAL; CHEMISTRY; CLASSIFICATION; EVOLUTION; GENETICS; ISOLATION AND PURIFICATION; MOLE (INSECTIVORA); MOLECULAR GENETICS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIROLOGY;

CRICETIDAE; HANTAVIRUS; MAMMALIA; MURIDAE; NEUROTRICHUS; NEUROTRICHUS GIBBSII; RODENTIA; SORICIDAE; SORICOMORPHA; TALPA EUROPAEA; TALPIDAE; UROTRICHUS TALPOIDES;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; BIOLOGICAL EVOLUTION; DNA PRIMERS; HANTAVIRUS; MOLECULAR SEQUENCE DATA; MOLES; PROTEIN STRUCTURE, SECONDARY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY, AMINO ACID; VIRAL PROTEINS;

EID: 67650264885     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0006149     Document Type: Article

References (75)

1. Schmaljohn CS, Dalrymple JM (1983) Analysis of Hantaan virus RNA: evidence for a new genus of Bunyaviridae. Virology 131: 482-491.
2. Schmaljohn CS, Hasty SE, Harrison SA, Dalrymple JM (1983) Characterization of Hantaan virions, the prototype virus of hemorrhagic fever with renal syndrome. J Infect Dis 148: 1005-1012.
3. Plyusnin A, Vapalahti O, Vaheri A (1996) Hantaviruses: genome structure, expression and evolution. J Gen Virol 77: 2677-2687.
4. Kukkonen SK, Vaheri A, Plyusnin A (2005) L protein, the RNA-dependent RNA polymerase of hantaviruses. Arch Virol 150: 533-556.
5. Lee HW, Lee P-W, Johnson KM (1978) Isolation of the etiologic agent of Korean hemorrhagic fever. J Infect Dis 137: 298-308.
6. Plyusnin A, Morzunov SP (2001) Virus evolution and genetic diversity of hantaviruses and their rodent hosts. Curr Top Microbiol Immunol 256: 47-75.
7. Yanagihara R (1990) Hantavirus infection in the United States: epizootiology and epidemiology. Rev Infect Dis 12: 449-457.
8. Yanagihara R, Gajdusek DC (1988) Hemorrhagic fever with renal syndrome: a historical perspective and review of recent advances. In: Gear JHS, ed. CRC Handbook of Viral and Rickettsial Hemorrhagic Fevers. Boca RatonFlorida: CRC Press, Inc. pp 151-188.
9. Duchin JS, Koster FT, Peters CJ, Simpson GL, Tempest B, et al. (1994) Hantavirus pulmonary syndrome: a clinical description of 17 patients with a newly recognized disease. N Engl J Med 330: 949-955.
10. Nichol ST, Spiropoulou CF, Morzunov S, Rollin PE, Ksiazek TG, et al. (1993) Genetic identification of a hantavirus associated with an outbreak of acute respiratory illness. Science 262: 914-917.
11. Clement J, McKenna P, Leirs H, Verhagen R, Lefevre A, et al. (1994) Hantavirus infections in rodents. In: Osterhaus A, ed. Virus Infections of Rodents and Lagomorphs. Amsterdam: Elsevier Science BV. pp 295-316.
12. Gavrilovskaya IN, Apekina NS, Myasnikov Yu A, Bernshtein AD, Ryltseva EV, et al. (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.
13. Tkachenko EA, Ivanov AP, Donets MA, Miasnikov YA, Ryltseva EV, et al. (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.
14. Carey DE, Reuben R, Panicker KN, Shope RE, Myers RM (1971) Thottapalayam virus: a presumptive arbovirus isolated from a shrew in India. Indian J Med Res 59: 1758-1760.
15. Song J-W, Baek LJ, Schmaljohn CS, Yanagihara R (2007) Thottapalayam virus, a prototype shrewborne hantavirus. Emerg Infect Dis 13: 980-985.
16. Yadav PD, Vincent MJ, Nichol ST (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.
17. Zeller HG, Karabatsos N, Calisher CH, Digoutte JP, Cropp CB, et al. (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.
18. Song J-W, Kang HJ, Gu SH, Moon SS, Bennett SN, et al. (2009) Characterization of Imjin virus, a newly isolated hantavirus from the Ussuri white-toothed shrew (Crocidura lasiura). J Virol 83: 6184-6191.
19. Song J-W, Gu SH, Bennett SN, Arai S, Puorger M, et al. (2007) Seewis virus, a genetically distinct hantavirus in the Eurasian common shrew (Sorex araneus). Virol J 4: 114.
20. Song J-W, Kang HJ, Song K-J, Truong TT, Bennett SN, et al. (2007) Newfound hantavirus in Chinese mole shrew, Vietnam. Emerg Infect Dis 13: 1784-1787.
21. Arai S, Song J-W, Sumibcay L, Bennett SN, Nerurkar VR, et al. (2007) Hantavirus in northern short-tailed shrew, United States. Emerg Infect Dis 13: 1420-1423.
22. Arai S, Bennett SN, Sumibcay L, Cook JA, Song J-W, et al. (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.
23. Klempa B, Fichet-Calvet E, Lecompte E, Auste B, Aniskin V, et al. (2007) Novel hantavirus sequences in shrew, Guinea. Emerg Infect Dis 13: 520-522.
24. Plyusnina A, Ibrahim IN, Plyusnin A (2009) A newly recognized hantavirus in the Asian house rat (Rattus tanezumi) in Indonesia. J Gen Virol 90: 205-209.
25. Sanchez AJ, Abbott KD, Nichol ST (2001) Genetic identification and characterization of limestone canyon virus, a unique Peromyscus-borne hantavirus. Virology 286: 345-353.
26. Vapalahti O, Lundkvist A, Fedorov V, Conroy CJ, Hirvonen S, et al. (1999) Isolation and characterization of a hantavirus from Lemmus sibiricus: evidence for host switch during hantavirus evolution. J Virol 73: 5586-5592.
27. Arai S, Ohdachi SD, Asakawa M, Kang HJ, Mocz G, et al. (2008) Molecular phylogeny of a newfound hantavirus in the Japanese shrew mole ( Urotrichus talpoides). Proc Natl Acad Sci USA 105: 16296-16301.
28. Kang HJ, Bennett SN, Dizney L, Sumibcay L, Arai S, et al. (2009) Host switch during evolution of a genetically distinct hantavirus in the American shrew mole (Neurotrichus gibbsii). Virology 388: 8-14.
29. Ramsden C, Holmes EC, Charleston MA (2009) Hantavirus evolution in relation to its rodent and insectivore hosts: no evidence for codivergence. Mol Biol Evol 26: 143-153.
30. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl Acids Res 22: 4673-4680.
31. Pond SL, Frost SD, Muse SV (2005) HyPhy: hypothesis testing using phylogenies. Bioinformatics 21: 676-679.
32. Padidam M, Sawyer S, Fauquet CM (1999) Possible emergence of new geminiviruses by frequent recombination. Virology 265: 218-225.
33. Martin DP, Posada D, Crandall KA, Williamson C (2005) A modified bootscan algorithm for automated identification of recombinant sequences and recombination breakpoints. AIDS Res Hum Retroviruses 21: 98-102.
34. Posada D, Crandall KA (2001) Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc Natl Acad Sci USA 98: 13757-13762.
35. Boni MF, Posada D, Feldman MW (2007) An exact nonparametric method for inferring mosaic structure in sequence triplets. Genetics 176: 1035-1047.
36. Martin D, Rybicki E (2000) RDP: detection of recombination amongst aligned sequences. Bioinformatics 16: 562-563.
37. Gibbs MJ, Armstrong JS, Gibbs AJ (2000) Sister-scanning: a Monte Carlo procedure for assessing signals in recombinant sequences. Bioinformatics 16: 573-582.
38. Combet C, Blanchet C, Geourjon C, Deleage G (2000) NPS" Network Protein Sequence Analysis. Trends Biochem Sci 25: 147-150.
39. Lupas A, Van Dyke M, Stock J (1991) Predicting coiled coils from protein sequences. Science 252: 1162-1164.
40. King RD, Sternberg MJ (1996) Identification and application of the concepts important for accurate and reliable protein secondary structure prediction. Protein Sci 5: 2298-2310.
41. Guermeur Y, Geourjon C, Gallinari P, Deléage G (1999) Improved performance in protein secondary structure prediction by inhomogeneous score combination. Bioinformatics 15: 413-421.
42. Rost B, Sander C (1993) Prediction of protein secondary structure at better than 70% accuracy. J Mol Biol 232: 584-599.
43. Frishman D, Argos P (1996) Incorporation of non-local interactions in protein secondary structure prediction from the amino acid sequence. Protein Eng 9: 133-142.
44. Swofford DL (2003) PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sunderland, Massachusetts: Sinauer Associates.
45. Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web servers. Syst Biol 57: 758-771.
46. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
47. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25: 1253-1256.
48. Charleston MA, Page RDM (1998) TreeMap 2.0b. Macintosh program for cophylogenetic analysis, 2.0b edition.
49. Charleston MA, Perkins SL (2006) Traversing the tangle: algorithms and applications for cophylogenetic studies. J Biomed Inform 39: 62-71.
50. Jackson AP, Charleston MA (2004) A cophylogenetic perspective of RNA-virus evolution. Mol Biol Evol 21: 45-57.
51. Irwin DM, Kocher TD, Wilson AC (1991) Evolution of the cytochrome b gene of mammals. J Mol Evol 32: 128-144.
52. Churchfield S (1990) The natural history of shrews. London: A&C Black Ltd. 178 p.
53. Gorman ML, Stone RD (1990) The natural history of moles. Ithaca: Cornell University Press. 138 p.
54. Gliwicz J, Taylor JRE (2002) Comparing life histories of shrews and rodents. Acta Theriol 1: 185-208.
55. Hinson ER, Shone SM, Zink MC, Glass GE, Klein SL (2004) Wounding: the primary mode of Seoul virus transmission among male Norway rats. Am J Trop Med Hyg 70: 310-317.
56. Easterbrook JD, Klein SL (2008) Immunological mechanisms mediating hantavirus persistence in rodent reservoirs. PLoS Pathog 4: e1000172.
57. Easterbrook JD, Zink MC, Klein SL (2007) Regulatory T cells enhance persistence of the zoonotic pathogen Seoul virus in its reservoir host. Proc Natl Acad Sci USA 104: 15502-15507.
58. Schountz T, Prescott J, Cogswell AC, Oko L, Mirowsky-Garcia K, et al. (2007) Regulatory T cell-like responses in deer mice persistently infected with Sin Nombre virus. Proc Natl Acad Sci USA 104: 15496-15501.
59. Hughes AL, Friedman R (2000) Evolutionary diversification of protein-coding genes of hantaviruses. Mol Biol Evol 17: 1558-1568.
60. Nemirov K, Henttonen H, Vaheri A, Plyusnin A (2002) Phylogenetic evidence for host switching in the evolution of hantaviruses carried by Apodemus mice. Virus Res 90: 207-215.
61. Zou Y, Wang JB, Gaowa HS, Yao LS, Hu GW, et al. (2008) Isolation and genetic characterization of hantaviruses carried by Microtus voles in China. J Med Virol 80: 680-688.
62. Zou Y, Xiao QY, Dong X, Lv W, Zhang SP, et al. (2008) Genetic analysis of hantaviruses carried by reed voles Microtus fortis in China. Virus Res 137: 122-128.
63. Plyusnina A, Laakkonen J, Niemimaa J, Nemirov K, Muruyeva G, et al. (2008) Genetic analysis of hantaviruses carried by Myodes and Microtus rodents in Buryatia. Virol J 5: 4.
64. Sánchez-Villagra MR, Horovitz I, Motokawa M (2006) A comprehensive morphological analysis of talpid moles (Mammalia) phylogenetic relationships. Cladistics 22: 59-88.
65. Shinohara A, Campbell KL, Suzuki H (2003) Molecular phylogenetic relationships of moles, shrew moles, and desmans from the new and old worlds. Mol Phylogenet Evol 27: 247-258.
66. Shinohara A, Suzuki H, Tsuchiya K, Zhang Y-P, Luo J, et al. (2004) Evolution and biogeography of talpid moles from continental East Asia and the Japanese islands inferred from mitochondrial and nuclear gene sequences. Zoolog Sci 21: 1177-1185.
67. Tsuchiya K, Suzuki H, Shinohara A, Harada M, Wakana S, et al. (2000) Molecular phylogeny of East Asian moles inferred from the sequence variation of the mitochondrial cytochrome b gene. Genes Genet Syst 75: 17-24.
68. Mills JN, Johnson JM, Ksiazek TG, Ellis BA, Rollin PE, et al. (1998) A survey of hantavirus antibody in small-mammal populations in selected United States National Parks. Am J Trop Med Hyg 58: 525-532.
69. Padula P, Figueroa R, Navarrete M, Pizarro E, Cadiz R, et al. (2004) Transmission study of Andes hantavirus infection in wild sigmodontine rodents. J Virol 78: 11972-11979.
70. Yates TL, Schmidly DJ (1978) Scalopus aquaticus. Mammalian Species 105: 1-4.
71. Alfadhli A, Steel E, Finlay L, Bachinger HP, Barklis E (2002) Hantavirus nucleocapsid protein coiled-coil domains. J Biol Chem 277: 27103-27108.
72. Boudko SP, Kuhn RJ, Rossmann MG (2007) The coiled-coil domain structure of the Sin Nombre virus nucleocapsid protein. J Mol Biol 366: 1538-1544.
73. Severson W, Xu X, Kuhn M, Senutovitch N, Thokala M, et al. (2005) Essential amino acids of the hantaan virus N protein in its interaction with RNA. J Virol 79: 10032-10039.
74. Xu X, Severson W, Villegas N, Schmaljohn CS, Jonsson CB (2002) The RNA binding domain of the hantaan virus N protein maps to a central, conserved region. J Virol 76: 3301-3308.
75. Alminaite A, Halttunen V, Kumar V, Vaheri A, Holm L, et al. (2006) Oligomerization of hantavirus nucleocapsid protein: analysis of the N-terminal coiled-coil domain. J Virol 80: 9073-9081.