1887

Abstract

This study identified the complete genomic sequence of four type 2 and type 3 human Saffold-like cardioviruses (SLCVs) isolated in Germany and Brazil. The secondary structures of the SLCV internal ribosome entry sites (IRESs) were deduced based on RNA base-pairing conservation and co-variation, using an established Theiler's murine encephalomyelitis virus (TMEV) IRES structure as a reference. The SLCV IRES was highly similar to that of TMEV, but motifs critical in TMEV for binding of the polypyrimidine tract-binding protein (PTB) were disrupted. In TMEV, corresponding alterations have been associated with reduced neurovirulence in mice. In the non-structural genome region, there was evidence of multiple intertypic recombination events between different SLCV types. Between viruses of the same type, recombination also occurred in the capsid-encoding genome region. There were apparently no recombination events between mouse TMEV and human SLCV. In another genus of the family , , natural recombination occurs strictly within species and can serve as an additional criterion for delimiting species. Accordingly, the results of this study suggest that SLCV and TMEV may represent distinct species within the genus .

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2010-06-01
2024-04-26
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References

  1. Abed, Y. & Boivin, G.(2008). New Saffold cardioviruses in 3 children, Canada. Emerg Infect Dis 14, 834–836.[CrossRef] [Google Scholar]
  2. Blinkova, O., Kapoor, A., Victoria, J., Jones, M., Wolfe, N., Naeem, A., Shaukat, S., Sharif, S., Alam, M. M. & other authors(2009). Cardioviruses are genetically diverse and cause common enteric infections in South Asian children. J Virol 83, 4631–4641.[CrossRef] [Google Scholar]
  3. Chen, H. H., Kong, W. P., Zhang, L., Ward, P. L. & Roos, R. P.(1995). A picornaviral protein synthesized out of frame with the polyprotein plays a key role in a virus-induced immune-mediated demyelinating disease. Nat Med 1, 927–931.[CrossRef] [Google Scholar]
  4. Chiu, C. Y., Greninger, A. L., Kanada, K., Kwok, T., Fischer, K. F., Runckel, C., Louie, J. K., Glaser, C. A., Yagi, S. & other authors(2008). Identification of cardioviruses related to Theiler's murine encephalomyelitis virus in human infections. Proc Natl Acad Sci U S A 105, 14124–14129.[CrossRef] [Google Scholar]
  5. Davis, M., Sagan, S. M., Pezacki, J. P., Evans, D. J. & Simmonds, P.(2008). Bioinformatic and physical characterizations of genome-scale ordered RNA structure in mammalian RNA viruses. J Virol 82, 11824–11836.[CrossRef] [Google Scholar]
  6. Drake, J. W.(1993). Rates of spontaneous mutation among RNA viruses. Proc Natl Acad Sci U S A 90, 4171–4175.[CrossRef] [Google Scholar]
  7. Drake, M. T., Riley, L. K. & Livingston, R. S.(2008). Differential susceptibility of SD and CD rats to a novel rat theilovirus. Comp Med 58, 458–464. [Google Scholar]
  8. Drexler, J. F., Luna, L. K., Stocker, A., Almeida, P. S., Ribeiro, T. C., Petersen, N., Herzog, P., Pedroso, C., Huppertz, H. I. & other authors(2008). Circulation of 3 lineages of a novel Saffold cardiovirus in humans. Emerg Infect Dis 14, 1398–1405.[CrossRef] [Google Scholar]
  9. Drummond, A. J. & Rambaut, A.(2007).beast: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7, 214[CrossRef] [Google Scholar]
  10. Duke, G. M., Hoffman, M. A. & Palmenberg, A. C.(1992). Sequence and structural elements that contribute to efficient encephalomyocarditis virus RNA translation. J Virol 66, 1602–1609. [Google Scholar]
  11. Gajdusek, D. C., Brown, P., Petrov, P. A. & Brown, P.(1970). V. Vilyuisk encephalitis in the Yakut Republic (U.S.S.R.). Am J Trop Med Hyg 19, 146–150. [Google Scholar]
  12. Hall, T. A.(1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41, 95–98. [Google Scholar]
  13. Harvala, H., Robertson, I., Chieochansin, T., McWilliam Leitch, E. C., Templeton, K. & Simmonds, P.(2009). Specific association of human parechovirus type 3 with sepsis and fever in young infants, as identified by direct typing of cerebrospinal fluid samples. J Infect Dis 199, 1753–1760.[CrossRef] [Google Scholar]
  14. Jones, M. S., Lukashov, V. V., Ganac, R. D. & Schnurr, D. P.(2007). Discovery of a novel human picornavirus in a stool sample from a pediatric patient presenting with fever of unknown origin. J Clin Microbiol 45, 2144–2150.[CrossRef] [Google Scholar]
  15. Kirkland, P. D., Gleeson, A. B., Hawkes, R. A., Naim, H. M. & Boughton, C. R.(1989). Human infection with encephalomyocarditis virus in New South Wales. Med J Aust 151, 176–178. [Google Scholar]
  16. Law, K. M. & Brown, T. D.(1990). The complete nucleotide sequence of the GDVII strain of Theiler's murine encephalomyelitis virus (TMEV). Nucleic Acids Res 18, 6707–6708.[CrossRef] [Google Scholar]
  17. Leitch, E. C., Harvala, H., Robertson, I., Ubillos, I., Templeton, K. & Simmonds, P.(2009). Direct identification of human enterovirus serotypes in cerebrospinal fluid by amplification and sequencing of the VP1 region. J Clin Virol 44, 119–124.[CrossRef] [Google Scholar]
  18. Liang, Z., Kumar, A. S., Jones, M. S., Knowles, N. J. & Lipton, H. L.(2008). Phylogenetic analysis of the species Theilovirus: emerging murine and human pathogens. J Virol 82, 11545–11554.[CrossRef] [Google Scholar]
  19. Librado, P. & Rozas, J.(2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.[CrossRef] [Google Scholar]
  20. Lole, K. S., Bollinger, R. C., Paranjape, R. S., Gadkari, D., Kulkarni, S. S., Novak, N. G., Ingersoll, R., Sheppard, H. W. & Ray, S. C.(1999). Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. J Virol 73, 152–160. [Google Scholar]
  21. Lu, C. Y., Lee, C. Y., Kao, C. L., Shao, W. Y., Lee, P. I., Twu, S. J., Yeh, C. C., Lin, S. C., Shih, W. Y. & other authors(2002). Incidence and case-fatality rates resulting from the 1998 enterovirus 71 outbreak in Taiwan. J Med Virol 67, 217–223.[CrossRef] [Google Scholar]
  22. Lukashev, A. N.(2005). Role of recombination in evolution of enteroviruses. Rev Med Virol 15, 157–167.[CrossRef] [Google Scholar]
  23. Lukashev, A. N., Lashkevich, V. A., Ivanova, O. E., Koroleva, G. A., Hinkkanen, A. E. & Ilonen, J.(2003). Recombination in circulating enteroviruses. J Virol 77, 10423–10431.[CrossRef] [Google Scholar]
  24. Lukashev, A. N., Lashkevich, V. A., Ivanova, O. E., Koroleva, G. A., Hinkkanen, A. E. & Ilonen, J.(2005). Recombination in circulating enterovirus B: independent evolution of structural and non-structural genome regions. J Gen Virol 86, 3281–3290.[CrossRef] [Google Scholar]
  25. Michiels, T., Jarousse, N. & Brahic, M.(1995). Analysis of the leader and capsid coding regions of persistent and neurovirulent strains of Theiler's virus. Virology 214, 550–558.[CrossRef] [Google Scholar]
  26. Myoung, J., Hou, W., Kang, B., Lyman, M. A., Kang, J. A. & Kim, B. S.(2007). The immunodominant CD8+ T cell epitope region of Theiler's virus in resistant C57BL/6 mice is critical for anti-viral immune responses, viral persistence, and binding to the host cells. Virology 360, 159–171.[CrossRef] [Google Scholar]
  27. Oberste, M. S., Maher, K. & Pallansch, M. A.(2004). Evidence for frequent recombination within species Human enterovirus B based on complete genomic sequences of all thirty-seven serotypes. J Virol 78, 855–867.[CrossRef] [Google Scholar]
  28. Ohara, Y., Stein, S., Fu, J. L., Stillman, L., Klaman, L. & Roos, R. P.(1988). Molecular cloning and sequence determination of DA strain of Theiler's murine encephalomyelitis viruses. Virology 164, 245–255.[CrossRef] [Google Scholar]
  29. Pallansch, M. A. & Roos, R. P.(2001).Enteroviruses: polioviruses, coxsackieviruses, echoviruses, and newer enteroviruses. In Fields Virology, 4th edn, pp. 724–743. Edited by D. M. Knipe & P. M. Howley. Philadelphia: Lippincott-Raven.
  30. Pestova, T. V., Kolupaeva, V. G., Lomakin, I. B., Pilipenko, E. V., Shatsky, I. N., Agol, V. I. & Hellen, C. U.(2001). Molecular mechanisms of translation initiation in eukaryotes. Proc Natl Acad Sci U S A 98, 7029–7036.[CrossRef] [Google Scholar]
  31. Pevear, D. C., Calenoff, M., Rozhon, E. & Lipton, H. L.(1987). Analysis of the complete nucleotide sequence of the picornavirus Theiler's murine encephalomyelitis virus indicates that it is closely related to cardioviruses. J Virol 61, 1507–1516. [Google Scholar]
  32. Pilipenko, E. V., Blinov, V. M., Romanova, L. I., Sinyakov, A. N., Maslova, S. V. & Agol, V. I.(1989). Conserved structural domains in the 5′-untranslated region of picornaviral genomes: an analysis of the segment controlling translation and neurovirulence. Virology 168, 201–209.[CrossRef] [Google Scholar]
  33. Pilipenko, E. V., Gmyl, A. P., Maslova, S. V., Belov, G. A., Sinyakov, A. N., Huang, M., Brown, T. D. & Agol, V. I.(1994). Starting window, a distinct element in the cap-independent internal initiation of translation on picornaviral RNA. J Mol Biol 241, 398–414.[CrossRef] [Google Scholar]
  34. Pilipenko, E. V., Gmyl, A. P., Maslova, S. V., Khitrina, E. V. & Agol, V. I.(1995). Attenuation of Theiler's murine encephalomyelitis virus by modifications of the oligopyrimidine/AUG tandem, a host-dependent translational cis element. J Virol 69, 864–870. [Google Scholar]
  35. Pilipenko, E. V., Viktorova, E. G., Guest, S. T., Agol, V. I. & Roos, R. P.(2001). Cell-specific proteins regulate viral RNA translation and virus-induced disease. EMBO J 20, 6899–6908.[CrossRef] [Google Scholar]
  36. Pritchard, A. E., Calenoff, M. A., Simpson, S., Jensen, K. & Lipton, H. L.(1992). A single base deletion in the 5′ noncoding region of Theiler's virus attenuates neurovirulence. J Virol 66, 1951–1958. [Google Scholar]
  37. Ronquist, F. & Huelsenbeck, J. P.(2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.[CrossRef] [Google Scholar]
  38. Sarmanova, E. S. & Chumachenko, G. G.(1960). Etiologic studies of Viliuisk encephalomyelitis. 3. Serologic studies. Curr Probl Med Virol 1, 216–219. [Google Scholar]
  39. Simmonds, P. & Smith, D. B.(1999). Structural constraints on RNA virus evolution. J Virol 73, 5787–5794. [Google Scholar]
  40. Simmonds, P. & Welch, J.(2006). Frequency and dynamics of recombination within different species of human enteroviruses. J Virol 80, 483–493.[CrossRef] [Google Scholar]
  41. Simmonds, P., Tuplin, A. & Evans, D. J.(2004). Detection of genome-scale ordered RNA structure (GORS) in genomes of positive-stranded RNA viruses: implications for virus evolution and host persistence. RNA 10, 1337–1351.[CrossRef] [Google Scholar]
  42. 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]
  43. Tauriainen, S., Martiskainen, M., Oikarinen, S., Lonnrot, M., Viskari, H., Ilonen, J., Simell, O., Knip, M. & Hyoty, H.(2007). Human parechovirus 1 infections in young children – no association with type 1 diabetes. J Med Virol 79, 457–462.[CrossRef] [Google Scholar]
  44. Thompson, J. D., Higgins, D. G. & Gibson, T. J.(1994).clustalw: 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]
  45. van Eyll, O. & Michiels, T.(2000). Influence of the Theiler's virus L* protein on macrophage infection, viral persistence, and neurovirulence. J Virol 74, 9071–9077.[CrossRef] [Google Scholar]
  46. Vladimirtsev, V. A., Nikitina, R. S., Renwick, N., Ivanova, A. A., Danilova, A. P., Platonov, F. A., Krivoshapkin, V. G., McLean, C. A., Masters, C. L. & other authors(2007). Family clustering of Viliuisk encephalomyelitis in traditional and new geographic regions. Emerg Infect Dis 13, 1321–1326.[CrossRef] [Google Scholar]
  47. Ward, C. D. & Flanegan, J. B.(1992). Determination of the poliovirus RNA polymerase error frequency at eight sites in the viral genome. J Virol 66, 3784–3793. [Google Scholar]
  48. Witso, E., Palacios, G., Cinek, O., Stene, L. C., Grinde, B., Janowitz, D., Lipkin, W. I. & Ronningen, K. S.(2006). High prevalence of human enterovirus A infections in natural circulation of human enteroviruses. J Clin Microbiol 44, 4095–4100.[CrossRef] [Google Scholar]
  49. Wolthers, K. C., Benschop, K. S., Schinkel, J., Molenkamp, R., Bergevoet, R. M., Spijkerman, I. J., Kraakman, H. C. & Pajkrt, D.(2008). Human parechoviruses as an important viral cause of sepsislike illness and meningitis in young children. Clin Infect Dis 47, 358–363.[CrossRef] [Google Scholar]
  50. Zoll, J., Erkens Hulshof, S., Lanke, K., Verduyn Lunel, F., Melchers, W. J., Schoondermark-van de Ven, E., Roivainen, M., Galama, J. M. & van Kuppeveld, F. J.(2009). Saffold virus, a human Theiler's-like cardiovirus, is ubiquitous and causes infection early in life. PLoS Pathog 5, e1000416[CrossRef] [Google Scholar]
  51. Zuker, M.(2003). Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31, 3406–3415.[CrossRef] [Google Scholar]
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