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Volume 66, Issue 7

Evolutionary changes in the capsid P2 region of Australian strains of the norovirus GII.Pe_GII.4 Free

Abstract

The protruding (P) 2 region of the norovirus capsid is thought to include hypervariable sites involved in receptor binding. This study examines the changes that occurred in the P2 region of GII.Pe_GII.4 norovirus in the course of its evolution from a precursor phase (2008–2009), to an intermediate phase (2010) and finally to an epidemic phase (2012–2015).

Twenty-two P2 region amino acid (aa) sequences (166 aa long) from all phases of the evolution of the virus were compared and the changes analysed.

Twenty sites in the P2 region underwent aa change and of these, 10 corresponded to previously proposed hypervariable sites and 10 to novel hypervariable sites. It was notable that aa changes at two sites, X and Y, only emerged as the epidemic phase progressed. 3D computer modelling of the P2 region indicated that neither X nor Y were in the uppermost ‘crown’, but further down in the ‘neck’ portion. The location of X and Y and the nature of aa change at Y suggest these sites were important in enhancing the structural integrity of the capsid, which in turn may have facilitated the longer term viability of the virus.

The current study helps establish the validity of previously proposed hypervariable sites in the P2 region as well as indicating new ones. It also provides quantitative and qualitative data on how these sites changed over the evolutionary history of a particular norovirus strain.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): amino acids , capsid , epidemic strain , evolution , norovirus and P2 region
© 2017 The Authors
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2017-07-01
2024-04-20
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References

  1. Aliabadi N, Lopman BA, Parashar UD, Hall AJ. Progress toward norovirus vaccines: considerations for further development and implementation in potential target populations. Expert Rev Vaccines 2015; 14:1241–1253 [View Article][PubMed]
     [Google Scholar]
  2. Green KY. Caliciviridae: The Noroviruses. In Knipe DM, Howley PM. (editors) Fields Virology, 6th ed. vol. 1 Philadelphia, PA: Wolters Kluwer/Lippincott Williams & Wilkins; 2013 pp. 582–608
     [Google Scholar]
  3. Vinjé J, Hamidjaja RA, Sobsey MD. Development and application of a capsid VP1 (region D) based reverse transcription PCR assay for genotyping of genogroup I and II noroviruses. J Virol Methods 2004; 116:109–117 [View Article][PubMed]
     [Google Scholar]
  4. Bok K, Green KY. Norovirus gastroenteritis in immunocompromised patients. N Engl J Med 2012; 367:2126–2132 [View Article][PubMed]
     [Google Scholar]
  5. Siebenga J, Kroneman A, Vennema H, Duizer E, Koopmans M. Food-borne viruses in Europe network report: the norovirus GII.4 2006b (for US named Minerva-like, for Japan Kobe034-like, for UK v6) variant now dominant in early seasonal surveillance. Euro Surveill 2008; 13:pii: 8009
     [Google Scholar]
  6. Kroneman A, Vega E, Vennema H, Vinjé J, White PA et al. Proposal for a unified norovirus nomenclature and genotyping. Arch Virol 2013; 158:2059–2068 [View Article][PubMed]
     [Google Scholar]
  7. Choi JM, Hutson AM, Estes MK, Prasad BV. Atomic resolution structural characterization of recognition of histo-blood group antigens by Norwalk virus. Proc Natl Acad Sci USA 2008; 105:9175–9180 [View Article][PubMed]
     [Google Scholar]
  8. Lindesmith LC, Beltramello M, Donaldson EF, Corti D, Swanstrom J et al. Immunogenetic mechanisms driving norovirus GII.4 antigenic variation. PLoS Pathog 2012; 8:e1002705 [View Article][PubMed]
     [Google Scholar]
  9. Bruggink LD, Dunbar NL, Marshall JA. Emergence of GII.e as a major ORF 1 norovirus genotype and its associated ORF 2 GII.4 variant forms. Infect Genet Evol 2014; 22:157–163 [View Article][PubMed]
     [Google Scholar]
  10. Bruggink LD, Dunbar NL, Catton MG, Marshall JA. Norovirus genotype diversity associated with gastroenteritis outbreaks in Victoria in 2013. Commun Dis Intell Q Rep 2015; 39:E34E41[PubMed]
     [Google Scholar]
  11. de Graaf M, van Beek J, Vennema H, Podkolzin AT, Hewitt J et al. Emergence of a novel GII.17 norovirus – end of the GII.4 era?. Euro Surveill 2015; 20:pii: 21178 [View Article]
     [Google Scholar]
  12. Bruggink L, Sameer R, Marshall J. Molecular and epidemiological characteristics of norovirus associated with community-based sporadic gastroenteritis incidents and norovirus outbreaks in Victoria, Australia, 2002–2007. Intervirology 2010; 53:167–172 [View Article][PubMed]
     [Google Scholar]
  13. Witlox KJ, Karapanagiotidis T, Bruggink LD, Marshall JA. The effect of fecal turbidity on norovirus detection by reverse transcriptase polymerase chain reaction. Diagn Microbiol Infect Dis 2010; 66:230–232 [View Article][PubMed]
     [Google Scholar]
  14. Witlox KJ, Nguyen TN, Bruggink LD, Catton MG, Marshall JA. A comparative evaluation of the sensitivity of two automated and two manual nucleic acid extraction methods for the detection of norovirus by RT-PCR. J Virol Methods 2008; 150:70–72 [View Article][PubMed]
     [Google Scholar]
  15. Bruggink LD, Oluwatoyin O, Sameer R, Witlox KJ, Marshall JA. Molecular and epidemiological features of gastroenteritis outbreaks involving genogroup I norovirus in Victoria, Australia, 2002-2010. J Med Virol 2012; 84:1437–1448 [View Article][PubMed]
     [Google Scholar]
  16. Kroneman A, Vennema H, Deforche K, V D Avoort H, Peñaranda S et al. An automated genotyping tool for enteroviruses and noroviruses. J Clin Virol 2011; 51:121–125 [View Article][PubMed]
     [Google Scholar]
  17. Höhne M, Niendorf S, Mas Marques A, Bock CT. Use of sequence analysis of the P2 domain for characterization of norovirus strains causing a large multistate outbreak of norovirus gastroenteritis in Germany 2012. Int J Med Microbiol 2015; 305:612–618 [View Article][PubMed]
     [Google Scholar]
  18. Bordoli L, Kiefer F, Arnold K, Benkert P, Battey J et al. Protein structure homology modeling using SWISS-MODEL workspace. Nat Protoc 2009; 4:1–13 [View Article][PubMed]
     [Google Scholar]
  19. Prasad BV, Hardy ME, Dokland T, Bella J, Rossmann MG et al. X-ray crystallographic structure of the Norwalk virus capsid. Science 1999; 286:287–290 [View Article][PubMed]
     [Google Scholar]
  20. Singh BK, Leuthold MM, Hansman GS. Human noroviruses' fondness for histo-blood group antigens. J Virol 2015; 89:2024–2040 [View Article][PubMed]
     [Google Scholar]
  21. Humphrey W, Dalke A, Schulten K. VMD: visual molecular dynamics. J Mol Graph 1996; 14:33–38 [View Article][PubMed]
     [Google Scholar]
  22. Roberts JA, Kuiper MJ, Thorley BR, Smooker PM, Hung A. Investigation of a predicted N-terminal amphipathic α-helix using atomistic molecular dynamics simulation of a complete prototype poliovirus virion. J Mol Graph Model 2012; 38:165–173 [View Article][PubMed]
     [Google Scholar]
  23. Frishman D, Argos P. Knowledge-based protein secondary structure assignment. Proteins 1995; 23:566–579 [View Article][PubMed]
     [Google Scholar]
  24. Debbink K, Donaldson EF, Lindesmith LC, Baric RS. Genetic mapping of a highly variable norovirus GII.4 blockade epitope: potential role in escape from human herd immunity. J Virol 2012; 86:1214–1226 [View Article][PubMed]
     [Google Scholar]
  25. Shanker S, Choi JM, Sankaran B, Atmar RL, Estes MK et al. Structural analysis of histo-blood group antigen binding specificity in a norovirus GII.4 epidemic variant: implications for epochal evolution. J Virol 2011; 85:8635–8645 [View Article][PubMed]
     [Google Scholar]
  26. de Rougemont A, Ruvoen-Clouet N, Simon B, Estienney M, Elie-Caille C et al. Qualitative and quantitative analysis of the binding of GII.4 norovirus variants onto human blood group antigens. J Virol 2011; 85:4057–4070 [View Article][PubMed]
     [Google Scholar]
  27. Kim JE, Lee SG, Cho HG, Han SH, Kang LH et al. Genetic analysis of the capsid region of norovirus GII.4 variants isolated in South Korea. J Microbiol 2014; 52:427–434 [View Article][PubMed]
     [Google Scholar]
  28. Xue L, Cai W, Wu Q, Kou X, Zhang J et al. Comparative genome analysis of a norovirus GII.4 strain GZ2013-L10 isolated from South China. Virus Genes 2016; 52:14–21 [View Article][PubMed]
     [Google Scholar]
  29. Kulkarni R, Patel A, Bhalla S, Chhabra P, Cherian S et al. Characterization of GII.4 noroviruses circulating among children with acute gastroenteritis in Pune, India: 2005-2013. Infect Genet Evol 2016; 37:163–173 [View Article][PubMed]
     [Google Scholar]
  30. Nelson DL, Cox MM. Lehninger Principles of Biochemistry, 3rd ed. New York, NY: Worth Publishers; 2000 pp. 118–120
     [Google Scholar]
  31. Qiao N, Wang XY, Liu L. Temporal evolutionary dynamics of norovirus GII.4 variants in China between 2004 and 2015. PLoS One 2016; 11:e0163166 [View Article][PubMed]
     [Google Scholar]
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Evolutionary changes in the capsid P2 region of Australian strains of the norovirus GII.Pe_GII.4
J. Med. Microbiol. 66, 1014 (2017); https://doi.org/10.1099/jmm.0.000531
/content/journal/jmm/10.1099/jmm.0.000531
/content/journal/jmm/10.1099/jmm.0.000531
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