1887

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Volume 90, Issue 4

Molecular characterization of a novel Ljungan virus (; ) reveals a fourth genotype and indicates ancestral recombination Free

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
2024-04-16
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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 797–855Edited by Schmidt N. J., Lennette D. A., Lennette E. T., Lennette E. H., Emmons R. W. 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 685–722Edited by Knipe D. M., Howley P. M., Griffin D. E., Lamb R. A., Martin M. A., Riozman B., Straus S. E. Philadelphia: Lippincott Williams & Wilkins;
     [Google Scholar]
  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 757–778Edited by Fauquet C. M., Mayo M. A., Maniloff J., Desselberger U., Ball L. A. London: Elsevier;
     [Google Scholar]
  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 57–86Edited by Miura R. M. Providence, RI: American Mathematical Society;
     [Google Scholar]
  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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Molecular characterization of a novel Ljungan virus (Parechovirus; Picornaviridae) reveals a fourth genotype and indicates ancestral recombination
J. Gen. Virol. 90, 843 (2009); https://doi.org/10.1099/vir.0.007948-0
/content/journal/jgv/10.1099/vir.0.007948-0
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