1887

Abstract

Ljungan virus (LV) was discovered 20 years ago in Swedish bank voles (, previously referred to as ) during the search for an infectious agent causing lethal myocarditis in young athletes. To date, the genomes of four LV isolates, including the prototype 87-012 strain, have been characterized. Three of these LV strains were isolated from bank voles trapped in Sweden. Sequence analysis of an American virus (M1146), isolated from a montane vole () in western USA, indicates that this strain represents a genotype that is different from the Swedish strains. Here, we present genomic analyses of a fifth LV strain (64-7855) isolated from a southern red-backed vole () trapped during arbovirus studies in New York state in the north-eastern USA in the 1960s. Sequence analysis of the 64-7855 genome showed an LV-like genome organization and sequence similarity to other LV strains. Genetic and phylogenetic analyses of the evolutionary relationship between the 64-7855 strain and other viruses within the family , including previously published LV strains, demonstrated that the 64-7855 strain constitutes a new genotype within the LV species. Analyses also showed that different regions of the 64-7855 genome have different phylogenetic relationships with other LV strains, indicating that previous recombination events have been involved in the evolution of this virus.

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2009-04-01
2019-11-12
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References

  1. Abed, Y. & Boivin, G. ( 2005; ). Molecular characterization of a Canadian human parechovirus (HPeV)-3 isolate and its relationship to other HPeVs. J Med Virol 77, 566–570.[CrossRef]
    [Google Scholar]
  2. Agol, V. I. ( 2002; ). Genomic instability in picornaviruses. Mol Biol (Mosk) 36, 286–295 (in Russian).
    [Google Scholar]
  3. Al-Sunaidi, M., Williams, C. H., Hughes, P. J., Schnurr, D. P. & Stanway, G. ( 2007; ). Analysis of a new human parechovirus allows the definition of parechovirus types and the identification of RNA structural domains. J Virol 81, 1013–1021.[CrossRef]
    [Google Scholar]
  4. Andersson, P., Edman, K. & Lindberg, A. M. ( 2002; ). Molecular analysis of the echovirus 18 prototype: evidence of interserotypic recombination with echovirus 9. Virus Res 85, 71–83.[CrossRef]
    [Google Scholar]
  5. Beaty, B. J., Calisher, C. H. & Shope, R. E. ( 1989; ). Arboviruses. In Diagnostic procedures for viral, rickettsial and chlamydial infections, pp. 797–855. Edited by N. J. Schmidt, D. A. Lennette, E. T. Lennette, E. H. Lennette & R. W. Emmons. Washington, DC: American Public Health Associations.
  6. Benschop, K. S. M., Schinkel, J., Luken, M. E., van den Broek, P. J. M., Beersma, M. F. C., Menelik, N., van Eijk, H. W. M., Zaaijer, H. L., VandenBroucke-Grauls, C. M. J. E. & other authors ( 2006; ). Fourth human parechovirus serotype. Emerg Infect Dis 12, 1572–1575.[CrossRef]
    [Google Scholar]
  7. Benschop, K. S. M., Williams, C. H., Wolthers, K. C., Stanway, G. & Simmonds, P. ( 2008; ). Widespread recombination within human parechoviruses: analysis of temporal dynamics and constraints. J Gen Virol 89, 1030–1035.[CrossRef]
    [Google Scholar]
  8. Blom, N., Hansen, J., Blaas, D. & Brunak, S. ( 1996; ). Cleavage site analysis in picornaviral polyproteins: discovering cellular targets by neural networks. Protein Sci 5, 2203–2216.[CrossRef]
    [Google Scholar]
  9. Boivin, G., Abed, Y. & Boucher, F. D. ( 2005; ). Human parechovirus 3 and neonatal infections. Emerg Infect Dis 11, 103–105.[CrossRef]
    [Google Scholar]
  10. Boni, M. F., Posada, D. & Feldman, M. W. ( 2007; ). An exact nonparametric method for inferring mosaic structure in sequence triplets. Genetics 176, 1035–1047.
    [Google Scholar]
  11. Carrillo, C., Tulman, E. R., Delhon, G., Lu, Z., Carreno, A., Vagnozzi, A., Kutish, G. F. & Rock, D. L. ( 2005; ). Comparative genomics of foot-and-mouth disease virus. J Virol 79, 6487–6504.[CrossRef]
    [Google Scholar]
  12. Clarke, B. E., Brown, A. L., Currey, K. M., Newton, S. E., Rowlands, D. J. & Carroll, A. R. ( 1987; ). Potential secondary and tertiary structure in the genomic RNA of foot and mouth disease virus. Nucleic Acids Res 15, 7067–7079.[CrossRef]
    [Google Scholar]
  13. De Rijk, P., Wuyts, J. & De Wachter, R. ( 2003; ). RnaViz 2: an improved representation of RNA secondary structure. Bioinformatics 19, 299–300.[CrossRef]
    [Google Scholar]
  14. Dobrikova, E. Y., Florez, P. & Gromeier, M. ( 2003; ). Structural determinants of insert retention of poliovirus expression vectors with recombinant IRES elements. Virology 311, 241–253.[CrossRef]
    [Google Scholar]
  15. Dougherty, W. G. & Semler, B. L. ( 1993; ). Expression of virus-encoded proteinases: functional and structural similarities with cellular enzymes. Microbiol Rev 57, 781–822.
    [Google Scholar]
  16. Ekström, J. O., Tolf, C., Edman, K. A. & Lindberg, A. M. ( 2007a; ). Physicochemical properties of the Ljungan virus prototype virion in different environments: inactivated by heat but resistant to acidic pH, detergents and non-physiological environments such as Virkon®-containing solutions. Microbiol Immunol 51, 841–850.[CrossRef]
    [Google Scholar]
  17. Ekström, J. O., Tolf, C., Fahlgren, C., Johansson, E. S., Arbrandt, G., Niklasson, B., Edman, K. A. & Lindberg, A. M. ( 2007b; ). Replication of Ljungan virus in cell culture: the genomic 5′-end, infectious cDNA clones and host cell response to viral infections. Virus Res 130, 129–139.[CrossRef]
    [Google Scholar]
  18. Etherington, G. J., Ring, S. M., Charleston, M. A., Dicks, J., Rayward-Smith, V. J. & Roberts, I. N. ( 2006; ). Tracing the origin and co-phylogeny of the caliciviruses. J Gen Virol 87, 1229–1235.[CrossRef]
    [Google Scholar]
  19. Ghazi, F., Hughes, P. J., Hyypiä, T. & Stanway, G. ( 1998; ). Molecular analysis of human parechovirus type 2 (formerly echovirus 23). J Gen Virol 79, 2641–2650.
    [Google Scholar]
  20. Gibbs, M. J., Armstrong, J. S. & Gibbs, A. J. ( 2000; ). Sister-Scanning: a Monte Carlo procedure for assessing signals in recombinant sequences. Bioinformatics 16, 573–582.[CrossRef]
    [Google Scholar]
  21. Goodfellow, I., Chaudhry, Y., Richardson, A., Meredith, J., Almond, J. W., Barclay, W. & Evans, D. J. ( 2000; ). Identification of a cis-acting replication element within the poliovirus coding region. J Virol 74, 4590–4600.[CrossRef]
    [Google Scholar]
  22. Goodfellow, I. G., Kerrigan, D. & Evans, D. J. ( 2003; ). Structure and function analysis of the poliovirus cis-acting replication element (CRE). RNA 9, 124–137.[CrossRef]
    [Google Scholar]
  23. Guindon, S. & Gascuel, O. ( 2003; ). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52, 696–704.[CrossRef]
    [Google Scholar]
  24. Henikoff, S. & Henikoff, J. G. ( 1992; ). Amino acid substitution matrices from protein blocks. Proc Natl Acad Sci U S A 89, 10915–10919.[CrossRef]
    [Google Scholar]
  25. Hofacker, I. L., Fekete, M. & Stadler, P. F. ( 2002; ). Secondary structure prediction for aligned RNA sequences. J Mol Biol 319, 1059–1066.[CrossRef]
    [Google Scholar]
  26. Holland, J., Spindler, K., Horodyski, F., Grabau, E., Nichol, S. & VandePol, S. ( 1982; ). Rapid evolution of RNA genomes. Science 215, 1577–1585.[CrossRef]
    [Google Scholar]
  27. Ito, M., Yamashita, T., Tsuzuki, H., Takeda, N. & Sakae, K. ( 2004; ). Isolation and identification of a novel human parechovirus. J Gen Virol 85, 391–398.[CrossRef]
    [Google Scholar]
  28. Johansson, S., Niklasson, B., Maizel, J., Gorbalenya, A. E. & Lindberg, A. M. ( 2002; ). Molecular analysis of three Ljungan virus isolates reveals a new, close-to-root lineage of the Picornaviridae with a cluster of two unrelated 2A proteins. J Virol 76, 8920–8930.[CrossRef]
    [Google Scholar]
  29. Johansson, E. S., Niklasson, B., Tesh, R. B., Shafren, D. R., da Rosa, A. P. A. T. & Lindberg, A. M. ( 2003; ). Molecular characterization of M1146, an American isolate of Ljungan virus (LV) reveals the presence of a new LV genotype. J Gen Virol 84, 837–844.[CrossRef]
    [Google Scholar]
  30. Johansson, E. S., Ekström, J. O., Shafren, D. R., Frisk, G., Hyypiä, T., Edman, K. & Lindberg, A. M. ( 2004; ). Cell culture propagation and biochemical analysis of the Ljungan virus prototype strain. Biochem Biophys Res Commun 317, 1023–1029.[CrossRef]
    [Google Scholar]
  31. Jones, D. T., Taylor, W. R. & Thornton, J. M. ( 1992; ). The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8, 275–282.
    [Google Scholar]
  32. Kozak, M. ( 1987; ). At least six nucleotides preceding the AUG initiator codon enhance translation in mammalian-cells. J Mol Biol 196, 947–950.[CrossRef]
    [Google Scholar]
  33. Le, S. Y., Chen, J. H., Sonenberg, N. & Maizel, J. V., Jr ( 1993; ). Conserved tertiary structural elements in the 5′ nontranslated region of cardiovirus, aphthovirus and hepatitis A virus RNAs. Nucleic Acids Res 21, 2445–2451.[CrossRef]
    [Google Scholar]
  34. Lindberg, A. M. & Johansson, S. ( 2002; ). Phylogenetic analysis of Ljungan virus and A-2 plaque virus, new members of the Picornaviridae. Virus Res 85, 61–70.[CrossRef]
    [Google Scholar]
  35. Lindberg, A. M., Andersson, P., Savolainen, C., Mulders, M. N. & Hovi, T. ( 2003; ). Evolution of the genome of human enterovirus B: incongruence between phylogenies of the VP1 and 3CD regions indicates frequent recombination within the species. J Gen Virol 84, 1223–1235.[CrossRef]
    [Google Scholar]
  36. Martin, D. & Rybicki, E. ( 2000; ). RDP: detection of recombination amongst aligned sequences. Bioinformatics 16, 562–563.[CrossRef]
    [Google Scholar]
  37. Martin, D. P., Posada, D., Crandall, K. A. & Williamson, C. ( 2005; ). A modified bootscan algorithm for automated identification of recombinant sequences and recombination breakpoints. AIDS Res Hum Retroviruses 21, 98–102.[CrossRef]
    [Google Scholar]
  38. Mathews, D. H. ( 2005; ). Predicting a set of minimal free energy RNA secondary structures common to two sequences. Bioinformatics 21, 2246–2253.[CrossRef]
    [Google Scholar]
  39. Mathews, D. H. & Turner, D. H. ( 2002; ). Dynalign: an algorithm for finding the secondary structure common to two RNA sequences. J Mol Biol 317, 191–203.[CrossRef]
    [Google Scholar]
  40. Mathews, D. H., Disney, M. D., Childs, J. L., Schroeder, S. J., Zuker, M. & Turner, D. H. ( 2004; ). Incorporating chemical modification constraints into a dynamic programming algorithm for prediction of RNA secondary structure. Proc Natl Acad Sci U S A 101, 7287–7292.[CrossRef]
    [Google Scholar]
  41. McKnight, K. L. & Lemon, S. M. ( 1998; ). The rhinovirus type 14 genome contains an internally located RNA structure that is required for viral replication. RNA 4, 1569–1584.[CrossRef]
    [Google Scholar]
  42. Needleman, S. B. & Wunsch, C. D. ( 1970; ). A general method applicable to the search for similarities in the amino acid sequence of two proteins. J Mol Biol 48, 443–453.[CrossRef]
    [Google Scholar]
  43. Niklasson, B., Hörnfeldt, B. & Lundman, B. ( 1998; ). Could myocarditis, insulin-dependent diabetes mellitus, and Guillain–Barré syndrome be caused by one or more infectious agents carried by rodents? Emerg Infect Dis 4, 187–193.[CrossRef]
    [Google Scholar]
  44. Niklasson, B., Kinnunen, L., Hörnfeldt, B., Hörling, J., Benemar, C., Hedlund, K. O., Matskova, L., Hyypiä, T. & Winberg, G. ( 1999; ). A new picornavirus isolated from bank voles (Clethrionomys glareolus). Virology 255, 86–93.[CrossRef]
    [Google Scholar]
  45. Niklasson, B., Samsioe, A., Papadogiannakis, N., Kawecki, A., Hörnfeldt, B., Saade, G. R. & Klitz, W. ( 2007; ). Association of zoonotic Ljungan virus with intrauterine fetal deaths. Birth Defects Res Part A Clin Mol Teratol 79, 488–493.[CrossRef]
    [Google Scholar]
  46. Oberste, M. S., Maher, K., Kilpatrick, D. R., Flemister, M. R., Brown, B. A. & Pallansch, M. A. ( 1999; ). Typing of human enteroviruses by partial sequencing of VP1. J Clin Microbiol 37, 1288–1293.
    [Google Scholar]
  47. Palmenberg, A. C. ( 1990; ). Proteolytic processing of picornaviral polyprotein. Annu Rev Microbiol 44, 603–623.[CrossRef]
    [Google Scholar]
  48. Palmenberg, A. C. & Sgro, J.-Y. ( 1997; ). Topological organization of picornaviral genomes: statistical prediction of RNA structural signals. Semin Virol 8, 231–241.[CrossRef]
    [Google Scholar]
  49. Paul, A. V., Rieder, E., Kim, D. W., van Boom, J. H. & Wimmer, E. ( 2000; ). Identification of an RNA hairpin in poliovirus RNA that serves as the primary template in the in vitro uridylylation of VPg. J Virol 74, 10359–10370.[CrossRef]
    [Google Scholar]
  50. Pilipenko, E. V., Blinov, V. M., Chernov, B. K., Dmitrieva, T. M. & Agol, V. I. ( 1989; ). Conservation of the secondary structure elements of the 5′-untranslated region of cardio- and aphthovirus RNAs. Nucleic Acids Res 17, 5701–5711.[CrossRef]
    [Google Scholar]
  51. Pond, S. L., Frost, S. D. & Muse, S. V. ( 2005; ). HyPhy: hypothesis testing using phylogenies. Bioinformatics 21, 676–679.[CrossRef]
    [Google Scholar]
  52. Posada, D. & Crandall, K. A. ( 1998; ). modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.[CrossRef]
    [Google Scholar]
  53. Posada, D. & Crandall, K. A. ( 2001; ). Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc Natl Acad Sci U S A 98, 13757–13762.[CrossRef]
    [Google Scholar]
  54. Racaniello, V. R. ( 2001; ). Picornaviridae: the viruses and their replication. In Fields Virology, 4th edn, pp. 685–722. Edited by D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Riozman & S. E. Straus. Philadelphia: Lippincott Williams & Wilkins.
  55. Rieder, E., Paul, A. V., Kim, D. W., van Boom, J. H. & Wimmer, E. ( 2000; ). Genetic and biochemical studies of poliovirus cis-acting replication element cre in relation to VPg uridylylation. J Virol 74, 10371–10380.[CrossRef]
    [Google Scholar]
  56. Rohll, J. B., Moon, D. H., Evans, D. J. & Almond, J. W. ( 1995; ). The 3′-untranslated region of picornavirus RNA: features required for efficient genome replication. J Virol 69, 7835–7844.
    [Google Scholar]
  57. Salminen, M. O., Carr, J. K., Burke, D. S. & McCutchan, F. E. ( 1995; ). Identification of breakpoints in intergenotypic recombinants of HIV type 1 by bootscanning. AIDS Res Hum Retroviruses 11, 1423–1425.[CrossRef]
    [Google Scholar]
  58. Simmonds, P. ( 2006; ). Recombination and selection in the evolution of picornaviruses and other mammalian positive-stranded RNA viruses. J Virol 80, 11124–11140.[CrossRef]
    [Google Scholar]
  59. Smith, J. M. ( 1992; ). Analyzing the mosaic structure of genes. J Mol Evol 34, 126–129.
    [Google Scholar]
  60. Stanway, G. & Hyypiä, T. ( 1999; ). Parechoviruses. J Virol 73, 5249–5254.
    [Google Scholar]
  61. Stanway, G., Brown, F., Christian, P., Hovi, T., Hyypiä, T., King, A. M. Q., Knowles, N. J., Lemon, S. M., Minor, P. D. & other authors ( 2005; ). Family Picornaviridae. In Virus Taxonomy, Eighth Report of the International Committee on Taxonomy of Viruses, pp. 757–778. Edited by C. M. Fauquet, M. A. Mayo, J. Maniloff, U. Desselberger & L. A. Ball. London: Elsevier.
  62. Strimmer, K. & von Haeseler, A. ( 1997; ). Likelihood-mapping: a simple method to visualize phylogenetic content of a sequence alignment. Proc Natl Acad Sci U S A 94, 6815–6819.[CrossRef]
    [Google Scholar]
  63. Tamura, K., Dudley, J., Nei, M. & Kumar, S. ( 2007; ). mega4: molecular evolutionary genetics analysis (mega) software version 4.0. Mol Biol Evol 24, 1596–1599.[CrossRef]
    [Google Scholar]
  64. Tavaré, S. ( 1986; ). Some probabilistic and statistical problems in the analysis of DNA sequences. In Some Mathematical Questions in Biology – DNA Sequence Analysis, pp. 57–86. Edited by R. M. Miura. Providence, RI: American Mathematical Society.
  65. Thompson, J. D., Higgins, D. G. & Gibson, T. J. ( 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.[CrossRef]
    [Google Scholar]
  66. Tolf, C., Ekström, J. O., Gullberg, M., Arbrandt, G., Niklasson, B., Frisk, G., Liljeqvist, J. A., Edman, K. & Lindberg, A. M. ( 2008; ). Characterization of polyclonal antibodies against the capsid proteins of Ljungan virus. J Virol Methods 150, 34–40.[CrossRef]
    [Google Scholar]
  67. Watanabe, K., Oie, M., Higuchi, M., Nishikawa, M. & Fujii, M. ( 2007; ). Isolation and characterization of novel human parechovirus from clinical samples. Emerg Infect Dis 13, 889–895.[CrossRef]
    [Google Scholar]
  68. Whitney, E., Roz, A. P. & Rayner, G. A. ( 1970; ). Two viruses isolated from rodents (Clethrionomys gapperi and Microtus pennsvlvanicus) trapped in St. Lawrence County, New York. J Wildl Dis 6, 48–55.[CrossRef]
    [Google Scholar]
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