1887

Abstract

In this novel study, we have for the first time identified evolutionarily conserved capsid residues in an individual chronically infected with norovirus (GGII.3). From 2000 to 2003, a total of 147 P1-1 and P2 capsid sequences were sequenced and investigated for evolutionarily conserved and functionally important residues by the evolutionary trace (ET) algorithm. The ET algorithm revealed more absolutely conserved residues (ACR) in the P1-1 domain (47/53, 88 %) as compared with the P2 domain (86/133, 64 %). The capsid P1-1 and P2 domains evolved in time-dependent manner, with a distinct break point observed between autumn/winter of year 2000 (isolates P1, P3 and P5) and spring to autumn of year 2001 (isolates P11, P13 and P15), which presumably coincided with a change of clinical symptoms. Furthermore, the ET analysis revealed a similar receptor-binding pattern as reported for Norwalk and VA387 strains, with the CS-4 and CS-5 patch (Norwalk strain) including residues 329 and 377 and residues 306 and 310, respectively, all being ACR in all partitions. Most interesting was that residues 343, 344, 345, 374, 390 and 391 of the proposed receptor A and B trisaccharide binding site (VA387 strain) within the P2 domain remained ACR in all partitions, presumably because there was no selective advantage to alter the histo blood group antigens (HBGA) receptor binding specificity. In conclusion, this study provides novel insights to the evolutionary process of norovirus during chronic infection.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.005082-0
2009-02-01
2019-11-13
Loading full text...

Full text loading...

/deliver/fulltext/jgv/90/2/432.html?itemId=/content/journal/jgv/10.1099/vir.0.005082-0&mimeType=html&fmt=ahah

References

  1. Bu, W., Mamedova, A., Tan, M., Xia, M., Jiang, X. & Hegde, R. S. ( 2008; ). Structural basis for the receptor binding specificity of the Norwalk virus. J Virol 82, 5340–5347.[CrossRef]
    [Google Scholar]
  2. Bull, R. A., Hansman, G. S., Clancy, L. E., Tanaka, M. M., Rawlinson, W. D. & White, P. A. ( 2005; ). Norovirus recombination in ORF1/ORF2 overlap. Emerg Infect Dis 11, 1079–1085.[CrossRef]
    [Google Scholar]
  3. Bull, R. A., Tanaka, M. M. & White, P. A. ( 2007; ). Norovirus recombination. J Gen Virol 88, 3347–3359.[CrossRef]
    [Google Scholar]
  4. Cao, S., Lou, Z., Tan, M., Chen, Y., Liu, Y., Zhang, Z., Zhang, X. C., Jiang, X., Li, X. & Rao, Z. ( 2007; ). Structural basis for the recognition of blood group trisaccharides by norovirus. J Virol 81, 5949–5957.[CrossRef]
    [Google Scholar]
  5. Chakravarty, S., Hutson, A. M., Estes, M. K. & Prasad, B. V. ( 2005; ). Evolutionary trace residues in noroviruses: importance in receptor binding, antigenicity, virion assembly, and strain diversity. J Virol 79, 554–568.[CrossRef]
    [Google Scholar]
  6. Domingo, E. & Holland, J. J. ( 1997; ). RNA virus mutations and fitness for survival. Annu Rev Microbiol 51, 151–178.[CrossRef]
    [Google Scholar]
  7. Domingo, E., Baranowski, E., Ruiz-Jarabo, C. M., Martin-Hernandez, A. M., Saiz, J. C. & Escarmis, C. ( 1998; ). Quasispecies structure and persistence of RNA viruses. Emerg Infect Dis 4, 521–527.[CrossRef]
    [Google Scholar]
  8. Eigen, M. ( 1993; ). Viral quasispecies. Sci Am 269, 42–49.
    [Google Scholar]
  9. Felsenstein, J. ( 1981; ). Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17, 368–376.[CrossRef]
    [Google Scholar]
  10. Felsenstein, J. ( 1985; ). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.[CrossRef]
    [Google Scholar]
  11. Forns, X., Purcell, R. H. & Bukh, J. ( 1999; ). Quasispecies in viral persistence and pathogenesis of hepatitis C virus. Trends Microbiol 7, 402–410.[CrossRef]
    [Google Scholar]
  12. Gallimore, C. I., Lewis, D., Taylor, C., Cant, A., Gennery, A. & Gray, J. J. ( 2004; ). Chronic excretion of a norovirus in a child with cartilage hair hypoplasia (CHH). J Clin Virol 30, 196–204.[CrossRef]
    [Google Scholar]
  13. Glass, R. I., Noel, J., Ando, T., Fankhauser, R., Belliot, G., Mounts, A., Parashar, U. D., Bresee, J. S. & Monroe, S. S. ( 2000; ). The epidemiology of enteric caliciviruses from humans: a reassessment using new diagnostics. J Infect Dis 181 (Suppl. 2), S254–S261.[CrossRef]
    [Google Scholar]
  14. Green, K. Y., Chanock, R. M. & Kapiakan, A. Z. ( 2001; ). Human caliciviruses. In Fields Virology, 4th edn, pp. 841–874. Baltimore, MD: Lippincott, Williams & Wilkins.
  15. 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]
  16. Hardy, M. E. ( 2005; ). Norovirus protein structure and function. FEMS Microbiol Lett 253, 1–8.[CrossRef]
    [Google Scholar]
  17. Hedlund, K. O., Rubilar-Abreu, E. & Svensson, L. ( 2000; ). Epidemiology of calicivirus infections in Sweden, 1994–1998. J Infect Dis 181 (Suppl. 2), S275–S280.[CrossRef]
    [Google Scholar]
  18. Innis, C. A., Shi, J. & Blundell, T. L. ( 2000; ). Evolutionary trace analysis of TGF-beta and related growth factors: implications for site-directed mutagenesis. Protein Eng 13, 839–847.[CrossRef]
    [Google Scholar]
  19. Jones, D. T. ( 1999; ). Protein secondary structure prediction based on position-specific scoring matrices. J Mol Biol 292, 195–202.[CrossRef]
    [Google Scholar]
  20. Le Pendu, J., Ruvoen-Clouet, N., Kindberg, E. & Svensson, L. ( 2006; ). Mendelian resistance to human norovirus infections. Semin Immunol 18, 375–386.[CrossRef]
    [Google Scholar]
  21. Lichtarge, O. & Sowa, M. E. ( 2002; ). Evolutionary predictions of binding surfaces and interactions. Curr Opin Struct Biol 12, 21–27.[CrossRef]
    [Google Scholar]
  22. Lichtarge, O., Bourne, H. R. & Cohen, F. E. ( 1996a; ). An evolutionary trace method defines binding surfaces common to protein families. J Mol Biol 257, 342–358.[CrossRef]
    [Google Scholar]
  23. Lichtarge, O., Bourne, H. R. & Cohen, F. E. ( 1996b; ). Evolutionarily conserved Galphabetagamma binding surfaces support a model of the G protein-receptor complex. Proc Natl Acad Sci U S A 93, 7507–7511.[CrossRef]
    [Google Scholar]
  24. Lindesmith, L., Moe, C., Marionneau, S., Ruvoen, N., Jiang, X., Lindblad, L., Stewart, P., LePendu, J. & Baric, R. ( 2003; ). Human susceptibility and resistance to Norwalk virus infection. Nat Med 9, 548–553.[CrossRef]
    [Google Scholar]
  25. Lindesmith, L. C., Donaldson, E. F., Lobue, A. D., Cannon, J. L., Zheng, D. P., Vinje, J. & Baric, R. S. ( 2008; ). Mechanisms of GII.4 norovirus persistence in human populations. PLoS Med 5, e31 [CrossRef]
    [Google Scholar]
  26. Martin, D. P., Williamson, C. & Posada, D. ( 2005; ). RDP2: recombination detection and analysis from sequence alignments. Bioinformatics 21, 260–262.[CrossRef]
    [Google Scholar]
  27. Nilsson, M., Hedlund, K. O., Thorhagen, M., Larson, G., Johansen, K., Ekspong, A. & Svensson, L. ( 2003; ). Evolution of human calicivirus RNA in vivo: accumulation of mutations in the protruding P2 domain of the capsid leads to structural changes and possibly a new phenotype. J Virol 77, 13117–13124.[CrossRef]
    [Google Scholar]
  28. Perriere, G. & Gouy, M. ( 1996; ). WWW-query: an on-line retrieval system for biological sequence banks. Biochimie 78, 364–369.[CrossRef]
    [Google Scholar]
  29. Phan, T. G., Kaneshi, K., Ueda, Y., Nakaya, S., Nishimura, S., Yamamoto, A., Sugita, K., Takanashi, S., Okitsu, S. & Ushijima, H. ( 2007; ). Genetic heterogeneity, evolution, and recombination in noroviruses. J Med Virol 79, 1388–1400.[CrossRef]
    [Google Scholar]
  30. Prasad, B. V., Hardy, M. E., Dokland, T., Bella, J., Rossmann, M. G. & Estes, M. K. ( 1999; ). X-ray crystallographic structure of the Norwalk virus capsid. Science 286, 287–290.[CrossRef]
    [Google Scholar]
  31. Rodriguez, F., Oliver, J. L., Marin, A. & Medina, J. R. ( 1990; ). The general stochastic model of nucleotide substitution. J Theor Biol 142, 485–501.[CrossRef]
    [Google Scholar]
  32. Rost, B., Yachdav, G. & Liu, J. ( 2004; ). The PredictProtein server. Nucleic Acids Res 32, W321–W326.[CrossRef]
    [Google Scholar]
  33. Saitou, N. & Nei, M. ( 1987; ). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4, 406–425.
    [Google Scholar]
  34. Siebenga, J. J., Vennema, H., Renckens, B., de Bruin, E., van der Veer, B., Siezen, R. J. & Koopmans, M. ( 2007; ). Epochal evolution of GGII.4 norovirus capsid proteins from 1995 to 2006. J Virol 81, 9932–9941.[CrossRef]
    [Google Scholar]
  35. Sowa, M. E., He, W., Slep, K. C., Kercher, M. A., Lichtarge, O. & Wensel, T. G. ( 2001; ). Prediction and conformation of a site critical for effector regulation of RGS domain activity. Nat Struct Biol 8, 234–237.[CrossRef]
    [Google Scholar]
  36. Tan, M. & Jiang, X. ( 2005; ). Norovirus and its histo-blood group antigen receptors: an answer to a historical puzzle. Trends Microbiol 13, 285–293.[CrossRef]
    [Google Scholar]
  37. Tan, M., Huang, P., Meller, J., Zhong, W., Farkas, T. & Jiang, X. ( 2003; ). Mutations within the P2 domain of norovirus capsid affect binding to human histo-blood group antigens: evidence for a binding pocket. J Virol 77, 12562–12571.[CrossRef]
    [Google Scholar]
  38. 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]
  39. Thorven, M., Grahn, A., Hedlund, K. O., Johansson, H., Wahlfrid, C., Larson, G. & Svensson, L. ( 2005; ). A homozygous nonsense mutation (428G→A) in the human secretor (FUT2) gene provides resistance to symptomatic norovirus (GGII) infections. J Virol 79, 15351–15355.[CrossRef]
    [Google Scholar]
  40. Worobey, M. & Holmes, E. C. ( 1999; ). Evolutionary aspects of recombination in RNA viruses. J Gen Virol 80, 2535–2543.
    [Google Scholar]
  41. Xia, X. & Xie, Z. ( 2001; ). dambe: software package for data analysis in molecular biology and evolution. J Hered 92, 371–373.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.005082-0
Loading
/content/journal/jgv/10.1099/vir.0.005082-0
Loading

Data & Media loading...

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error