1887

Journal of General Virology header logo

Volume 95, Issue 7

Relationship between genotypes and serotypes of genogroup 1 recoviruses: a model for human norovirus antigenic diversity Free

Abstract

Human norovirus (NoV) research greatly relies on cell culture-propagable surrogate caliciviruses, including murine NoVs and the prototype ‘recovirus’ (ReCV), Tulane virus. However, the extreme biological diversity of human NoVs cannot be modelled by a uniform group of viruses or single isolate. Based on a diverse group of recently described ReCVs, a more advanced model reflecting human NoV biological diversity is currently under development. Here, we have reported the genotypic and serotypic relationships among 10 G1 ReCV isolates, including Tulane virus and nine other recent cell culture-adapted strains. Based on the amino acid sequences of virus capsid protein, VP1, and classification constraints established for NoVs, G1 ReCVs were separated into three genotypes, with variable organization of the three open reading frames. Interestingly, cross-neutralization plaque assays revealed the existence of four distinct serotypes, two of which were detected among the G1.2 strains. The amino acid (aa) difference between the two G1.2 ReCV serotypes (12%) was less than the minimum 13 % difference established between NoV genotypes. Interestingly, one of the G1.3 ReCVs was equally neutralized by antisera raised against the G1.3 (6 % aa difference) and G1.1 (25 % aa difference) representative strains. These results imply the existence of a large number of human NoV serotypes, but also shared cross-neutralization epitopes between some strains of different genotypes. In conclusion, the newly developed ReCV surrogate model can be applied to address biologically relevant questions pertaining to enteric CV diversity.

  • Received:
  • Accepted:
  • Published Online:
© 2014 The Authors
Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.064675-0
2014-07-01
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/jgv/95/7/1469.html?itemId=/content/journal/jgv/10.1099/vir.0.064675-0&mimeType=html&fmt=ahah

References

  1. Bok K., Parra G. I., Mitra T., Abente E., Shaver C. K., Boon D., Engle R., Yu C., Kapikian A. Z. other authors 2011; Chimpanzees as an animal model for human norovirus infection and vaccine development. Proc Natl Acad Sci U S A 108:325–330 [View Article][PubMed]
     [Google Scholar]
  2. Choi J. M., Hutson A. M., Estes M. K., Prasad B. V. 2008; Atomic resolution structural characterization of recognition of histo-blood group antigens by Norwalk virus. Proc Natl Acad Sci U S A 105:9175–9180 [View Article][PubMed]
     [Google Scholar]
  3. Committee on Enteroviruses 1962; Classification of human enteroviruses. Virology 16:501–504 [View Article]
     [Google Scholar]
  4. Cowen B. S., Hitchner S. B. 1975; Serotyping of avian infectious bronchitis viruses by the virus-neutralization test. Avian Dis 19:583–595 [View Article][PubMed]
     [Google Scholar]
  5. Debbink K., Lindesmith L. C., Donaldson E. F., Baric R. S. 2012; Norovirus immunity and the great escape. PLoS Pathog 8:e1002921 [View Article][PubMed]
     [Google Scholar]
  6. DiCaprio E., Ma Y., Purgianto A., Hughes J., Li J. 2012; Internalization and dissemination of human norovirus and animal caliciviruses in hydroponically grown romaine lettuce. Appl Environ Microbiol 78:6143–6152 [View Article][PubMed]
     [Google Scholar]
  7. Farkas T., Sestak K., Wei C., Jiang X. 2008; Characterization of a rhesus monkey calicivirus representing a new genus of Caliciviridae . J Virol 82:5408–5416 [View Article][PubMed]
     [Google Scholar]
  8. Farkas T., Cross R. W., Hargitt E. III, Lerche N. W., Morrow A. L., Sestak K. 2010a; Genetic diversity and histo-blood group antigen interactions of rhesus enteric caliciviruses. J Virol 84:8617–8625 [View Article][PubMed]
     [Google Scholar]
  9. Farkas T., Dufour J., Jiang X., Sestak K. 2010b; Detection of norovirus-, sapovirus- and rhesus enteric calicivirus-specific antibodies in captive juvenile macaques. J Gen Virol 91:734–738 [View Article][PubMed]
     [Google Scholar]
  10. Farkas T., Falkenstein K. P., Bohm R. P., Pecotte J., Sestak K. 2012; High incidence of rhesus enteric calicivirus infections and diarrhea in captive juvenile macaques: a likely association. J Med Primatol 41:325–328 [View Article][PubMed]
     [Google Scholar]
  11. Frenck R., Bernstein D. I., Xia M., Huang P., Zhong W., Parker S., Dickey M., McNeal M., Jiang X. 2012; Predicting susceptibility to norovirus GII.4 by use of a challenge model involving humans. J Infect Dis 206:1386–1393 [View Article][PubMed]
     [Google Scholar]
  12. Green K. Y. 2013; Caliciviridae: the noroviruses. In Fields Virology, 6th edn. vol. 1 pp 582–608 Edited by Knipe D. M., Howley P. M. Philadelphia: Lippincott Williams & Wilkins;
     [Google Scholar]
  13. Hall A. J., Curns A. T., McDonald L. C., Parashar U. D., Lopman B. A. 2012; The roles of Clostridium difficile and norovirus among gastroenteritis-associated deaths in the United States, 1999–2007. Clin Infect Dis 55:216–223 [View Article][PubMed]
     [Google Scholar]
  14. Handley S. A., Thackray L. B., Zhao G., Presti R., Miller A. D., Droit L., Abbink P., Maxfield L. F., Kambal A. other authors 2012; Pathogenic simian immunodeficiency virus infection is associated with expansion of the enteric virome. Cell 151:253–266 [View Article][PubMed]
     [Google Scholar]
  15. Hirneisen K. A., Kniel K. E. 2013a; Norovirus surrogate survival on spinach during preharvest growth. Phytopathology 103:389–394 [View Article][PubMed]
     [Google Scholar]
  16. Hirneisen K. A., Kniel K. E. 2013b; Comparing human norovirus surrogates: murine norovirus and Tulane virus. J Food Prot 76:139–143 [View Article][PubMed]
     [Google Scholar]
  17. Huang P. W., Farkas T., Zhong W., Tan M., Thornton S., Morrow A. L., Jiang X. 2005; Norovirus and histo-blood group antigens: demonstration of a wide spectrum of strain specificities and classification of two major binding groups among multiple binding patterns. J Virol 79:6714–6722 [View Article][PubMed]
     [Google Scholar]
  18. Kapikian A. Z., Conan R. M., Hamparian V. V., Chanock R. M., Chapple P. J., Dick E. C., Fenters J. D., Gwaltney J. M., Hamre D. 1967; Rhinoviruses: a numbering system. Nature 213:761–763 [View Article][PubMed]
     [Google Scholar]
  19. Kapikian A. Z., Wyatt R. G., Dolin R., Thornhill T. S., Kalica A. R., Chanock R. M. 1972; Visualization by immune electron microscopy of a 27-nm particle associated with acute infectious nonbacterial gastroenteritis. J Virol 10:1075–1081[PubMed]
     [Google Scholar]
  20. Katpally U., Wobus C. E., Dryden K., Virgin H. W. IV, Smith T. J. 2008; Structure of antibody-neutralized murine norovirus and unexpected differences from viruslike particles. J Virol 82:2079–2088 [View Article][PubMed]
     [Google Scholar]
  21. Kelley L. A., Sternberg M. J. E. 2009; Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4:363–371 [View Article][PubMed]
     [Google Scholar]
  22. Kringelum J. V., Lundegaard C., Lund O., Nielsen M. 2012; Reliable B cell epitope predictions: impacts of method development and improved benchmarking. PLOS Comput Biol 8:e1002829 [View Article][PubMed]
     [Google Scholar]
  23. Kroneman A., Vega E., Vennema H., Vinjé J., White P. A., Hansman G., Green K., Martella V., Katayama K., Koopmans M. 2013; Proposal for a unified norovirus nomenclature and genotyping. Arch Virol 158:2059–2068 [View Article][PubMed]
     [Google Scholar]
  24. Larsen J. E., Lund O., Nielsen M. 2006; Improved method for predicting linear B-cell epitopes. Immunome Res 2:2 [View Article][PubMed]
     [Google Scholar]
  25. Li X., Ye M., Neetoo H., Golovan S., Chen H. 2013; Pressure inactivation of Tulane virus, a candidate surrogate for human norovirus and its potential application in food industry. Int J Food Microbiol 162:37–42 [View Article][PubMed]
     [Google Scholar]
  26. Lindesmith L., Moe C., Marionneau S., Ruvoen N., Jiang X., Lindblad L., Stewart P., LePendu J., Baric R. S. 2003; Human susceptibility and resistance to Norwalk virus infection. Nat Med 9:548–553 [View Article][PubMed]
     [Google Scholar]
  27. Lindesmith L. C., Beltramello M., Donaldson E. F., Corti D., Swanstrom J., Debbink K., Lanzavecchia A., Baric R. S. 2012; Immunogenetic mechanisms driving norovirus GII.4 antigenic variation. PLoS Pathog 8:e1002705 [View Article][PubMed]
     [Google Scholar]
  28. Lindesmith L. C., Costantini V., Swanstrom J., Debbink K., Donaldson E. F., Vinjé J., Baric R. S. 2013; Emergence of a norovirus GII.4 strain correlates with changes in evolving blockade epitopes. J Virol 87:2803–2813 [View Article][PubMed]
     [Google Scholar]
  29. Lopman B. A., Hall A. J., Curns A. T., Parashar U. D. 2011; Increasing rates of gastroenteritis hospital discharges in US adults and the contribution of norovirus, 1996–2007. Clin Infect Dis 52:466–474 [View Article][PubMed]
     [Google Scholar]
  30. McFadden N., Bailey D., Carrara G., Benson A., Chaudhry Y., Shortland A., Heeney J., Yarovinsky F., Simmonds P. other authors 2011; Norovirus regulation of the innate immune response and apoptosis occurs via the product of the alternative open reading frame 4. PLoS Pathog 7:e1002413 [View Article][PubMed]
     [Google Scholar]
  31. Oliver S. L., Batten C. A., Deng Y., Elschner M., Otto P., Charpilienne A., Clarke I. N., Bridger J. C., Lambden P. R. 2006; Genotype 1 and genotype 2 bovine noroviruses are antigenically distinct but share a cross-reactive epitope with human noroviruses. J Clin Microbiol 44:992–998 [CrossRef]
     [Google Scholar]
  32. Parker T. D., Kitamoto N., Tanaka T., Hutson A. M., Estes M. K. 2005; Identification of Genogroup I and Genogroup II broadly reactive epitopes on the norovirus capsid. J Virol 79:7402–7409 [View Article][PubMed]
     [Google Scholar]
  33. Parra G. I., Azure J., Fischer R., Bok K., Sandoval-Jaime C., Sosnovtsev S. V., Sander P., Green K. Y. 2013; Identification of a broadly cross-reactive epitope in the inner shell of the norovirus capsid. PLoS ONE 8:e67592 [View Article][PubMed]
     [Google Scholar]
  34. Richards G. P. 2012; Critical review of norovirus surrogates in food safety research: rationale for considering volunteer studies. Food Environ Virol 4:6–13 [View Article][PubMed]
     [Google Scholar]
  35. Scallan E., Hoekstra R. M., Angulo F. J., Tauxe R. V., Widdowson M. A., Roy S. L., Jones J. L., Griffin P. M. 2011; Foodborne illness acquired in the United States–major pathogens. Emerg Infect Dis 17:7–15 [View Article][PubMed]
     [Google Scholar]
  36. Sestak K., Feely S., Fey B., Dufour J., Hargitt E., Alvarez X., Pahar B., Gregoricus N., Vinjé J., Farkas T. 2012; Experimental inoculation of juvenile rhesus macaques with primate enteric caliciviruses. PLoS ONE 7:e37973 [View Article][PubMed]
     [Google Scholar]
  37. Shanker S., Choi J. M., Sankaran B., Atmar R. L., Estes M. K., Prasad B. V. 2011; Structural analysis of histo-blood group antigen binding specificity in a norovirus GII.4 epidemic variant: implications for epochal evolution. J Virol 85:8635–8645 [View Article][PubMed]
     [Google Scholar]
  38. Smith A. W., Berry E. S., Skilling D. E., Barlough J. E., Poet S. E., Berke T., Mead J., Matson D. O. 1998; In vitro isolation and characterization of a calicivirus causing a vesicular disease of the hands and feet. Clin Infect Dis 26:434–439 [View Article][PubMed]
     [Google Scholar]
  39. Smits S. L., Rahman M., Schapendonk C. M., van Leeuwen M., Faruque A. S., Haagmans B. L., Endtz H. P., Osterhaus A. D. 2012; Calicivirus from novel Recovirus genogroup in human diarrhea, Bangladesh. Emerg Infect Dis 18:1192–1195 [View Article][PubMed]
     [Google Scholar]
  40. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. 2011; mega5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739 [View Article][PubMed]
     [Google Scholar]
  41. Vashist S., Bailey D., Putics A., Goodfellow I. 2009; Model systems for the study of human norovirus Biology. Future Virol 4:353–367 [View Article][PubMed]
     [Google Scholar]
  42. Wobus C. E., Thackray L. B., Virgin H. W. IV 2006; Murine norovirus: a model system to study norovirus biology and pathogenesis. J Virol 80:5104–5112 [View Article][PubMed]
     [Google Scholar]
  43. Wyatt R. G., Greenberg H. B., James W. D., Pittman A. L., Kalica A. R., Flores J., Chanock R. M., Kapikian A. Z. 1982; Definition of human rotavirus serotypes by plaque reduction assay. Infect Immun 37:110–115[PubMed]
     [Google Scholar]
  44. Zheng D. P., Ando T., Fankhauser R. L., Beard R. S., Glass R. I., Monroe S. S. 2006; Norovirus classification and proposed strain nomenclature. Virology 346:312–323 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.064675-0
Loading
Relationship between genotypes and serotypes of genogroup 1 recoviruses: a model for human norovirus antigenic diversity
J. Gen. Virol. 95, 1469 (2014); https://doi.org/10.1099/vir.0.064675-0
/content/journal/jgv/10.1099/vir.0.064675-0
/content/journal/jgv/10.1099/vir.0.064675-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

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