1887

Abstract

Human noroviruses are one of the major causes of acute gastroenteritis worldwide. Due to the lack of an efficient human norovirus cell culture system coupled with an animal model, human norovirus research mainly relies on human volunteer studies and surrogate models. Current models either utilize human norovirus-infected animals including the gnotobiotic pig or calf and the chimpanzee models, or employ other members of the family including cell culture propagable surrogate caliciviruses such as the feline calicivirus, murine norovirus and most recently the Tulane virus. One of the major features of human noroviruses is their extreme biological diversity, including genetic, antigenic and histo-blood group antigen binding diversity, and possible differences of virulence and environmental stability. This extreme biological diversity and its effect on intervention/prevention strategies cannot be modelled by uniform groups of surrogates, much less by single isolates. Tulane virus, the prototype recovirus strain, was discovered in 2008. Since then, several other novel recoviruses have been described and cell culture adapted. Recent studies indicate that the epidemiology, the biological features and diversity of recoviruses and the course of infection and clinical disease in recovirus-infected macaques more closely reflect those properties of human noroviruses than any of the current surrogates. This review aims to summarize what is currently known about recoviruses, highlight their biological similarities to human noroviruses and discuss applications of the model in addressing questions relevant for human norovirus research.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000020
2015-07-01
2019-12-06
Loading full text...

Full text loading...

/deliver/fulltext/jgv/96/7/1504.html?itemId=/content/journal/jgv/10.1099/jgv.0.000020&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. et al. ( 2011; ). Chimpanzees as an animal model for human norovirus infection and vaccine development. . Proc Natl Acad Sci U S A 108:, 325–330. [CrossRef] [PubMed]
    [Google Scholar]
  2. Caddy S., Breiman A., le Pendu J., Goodfellow I.. ( 2014; ). Genogroup IV and VI canine noroviruses interact with histo-blood group antigens. . J Virol 88:, 10377–10391. [CrossRef] [PubMed]
    [Google Scholar]
  3. Chan M. C., Ho W. S., Sung J. J.. ( 2011; ). In vitro whole-virus binding of a norovirus genogroup II genotype 4 strain to cells of the lamina propria and Brunner’s glands in the human duodenum. . J Virol 85:, 8427–8430. [CrossRef] [PubMed]
    [Google Scholar]
  4. Cheetham S., Souza M., Meulia T., Grimes S., Han M. G., Saif L. J.. ( 2006; ). Pathogenesis of a genogroup II human norovirus in gnotobiotic pigs. . J Virol 80:, 10372–10381. [CrossRef] [PubMed]
    [Google Scholar]
  5. Cromeans T., Park G. W., Costantini V., Lee D., Wang Q., Farkas T., Lee A., Vinjé J..( 2014; ). Comprehensive comparison of cultivable norovirus surrogates in response to different inactivation and disinfection treatments. Appl Environ Microbiol 80, 5743–5751. [CrossRef] [PubMed]
  6. Debbink K, Lindesmith L. C., Donaldson E. F., Baric R. S.. ( 2012; ). Norovirus immunity and the great escape. PLoS Pathog 8, e1002921. [CrossRef] [PubMed]
  7. Degen L. P., Phillips S. F.. ( 1996; ). Variability of gastrointestinal transit in healthy women and men. . Gut 39:, 299–305. [CrossRef] [PubMed]
    [Google Scholar]
  8. Farkas T., Wong Ping Lun C.. ( 2014; ). Prevalence of recovirus-neutralizing antibodies in human serum samples. . J Clin Microbiol 52:, 3088–3090. [CrossRef] [PubMed]
    [Google Scholar]
  9. 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. [CrossRef] [PubMed]
    [Google Scholar]
  10. Farkas T., Cross R. W., Hargitt E. III, Lerche N. W., Morrow A. L., Sestak K.. ( 2010; a). Genetic diversity and histo-blood group antigen interactions of rhesus enteric caliciviruses. . J Virol 84:, 8617–8625. [CrossRef] [PubMed]
    [Google Scholar]
  11. Farkas T., Dufour J., Jiang X., Sestak K.. ( 2010; b). Detection of norovirus-, sapovirus- and rhesus enteric calicivirus-specific antibodies in captive juvenile macaques. . J Gen Virol 91:, 734–738. [CrossRef] [PubMed]
    [Google Scholar]
  12. 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. [CrossRef] [PubMed]
    [Google Scholar]
  13. Farkas T., Lun C. W. P., Fey B.. ( 2014; ). Relationship between genotypes and serotypes of genogroup 1 recoviruses: a model for human norovirus antigenic diversity. . J Gen Virol 95:, 1469–1478. [CrossRef] [PubMed]
    [Google Scholar]
  14. Fastier L. B.. ( 1957; ). A new feline virus isolated in tissue culture. . Am J Vet Res 18:, 382–389.[PubMed]
    [Google Scholar]
  15. 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. [CrossRef] [PubMed]
    [Google Scholar]
  16. Friesema I. H., Vennema H., Heijne J. C., de Jager C. M., Teunis P. F., van der Linde R., Duizer E., van Duynhoven Y. T.. ( 2009; ). Differences in clinical presentation between norovirus genotypes in nursing homes. . J Clin Virol 46:, 341–344. [CrossRef] [PubMed]
    [Google Scholar]
  17. González-Reyes S., García-Manso A., del Barrio G., Dalton K. P., González-Molleda L., Arrojo-Fernández J., Nicieza I., Parra F.. ( 2009; ). Role of annexin A2 in cellular entry of rabbit vesivirus. . J Gen Virol 90:, 2724–2730. [CrossRef] [PubMed]
    [Google Scholar]
  18. Green K. Y.. ( 2013; ). Caliciviridae: the noroviruses. . In Fields Virology, , 6th edn., pp. 582–608. Edited by Knipe D. M., Howley P. M... Philadelphia, PA:: Lippincott Williams & Wilkins;.
    [Google Scholar]
  19. Guix S., Asanaka M., Katayama K., Crawford S. E., Neill F. H., Atmar R. L., Estes M. K.. ( 2007; ). Norwalk virus RNA is infectious in mammalian cells. . J Virol 81:, 12238–12248. [CrossRef] [PubMed]
    [Google Scholar]
  20. 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. [CrossRef] [PubMed]
    [Google Scholar]
  21. Handley S. A., Thackray L. B., Zhao G., Presti R., Miller A. D., Droit L., Abbink P., Maxfield L. F., Kambal A. et al. ( 2012; ). Pathogenic simian immunodeficiency virus infection is associated with expansion of the enteric virome. . Cell 151:, 253–266. [CrossRef] [PubMed]
    [Google Scholar]
  22. 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. [CrossRef] [PubMed]
    [Google Scholar]
  23. Jones M. K., Watanabe M., Zhu S., Graves C. L., Keyes L. R., Grau K. R., Gonzalez-Hernandez M. B., Iovine N. M., Wobus C. E. et al. ( 2014; ). Enteric bacteria promote human and mouse norovirus infection of B cells. . Science 346:, 755–759. [CrossRef] [PubMed]
    [Google Scholar]
  24. 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]
  25. Karst S. M., Wobus C. E., Lay M., Davidson J., Virgin H. W. IV. ( 2003; ). STAT1-dependent innate immunity to a Norwalk-like virus. . Science 299:, 1575–1578. [CrossRef] [PubMed]
    [Google Scholar]
  26. Kirby A. E., Shi J., Montes J., Lichtenstein M., Moe C. L.. ( 2014; ). Disease course and viral shedding in experimental Norwalk virus and Snow Mountain virus infection. . J Med Virol 86:, 2055–2064.[PubMed]
    [Google Scholar]
  27. Kong F., Singh R. P.. ( 2008; ). Disintegration of solid foods in human stomach. . J Food Sci 73:, R67–R80. [CrossRef] [PubMed]
    [Google Scholar]
  28. 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. [CrossRef] [PubMed]
    [Google Scholar]
  29. Lay M. K., Atmar R. L., Guix S., Bharadwaj U., He H., Neill F. H., Sastry K. J., Yao Q., Estes M. K.. ( 2010; ). Norwalk virus does not replicate in human macrophages or dendritic cells derived from the peripheral blood of susceptible humans. . Virology 406:, 1–11. [CrossRef] [PubMed]
    [Google Scholar]
  30. Le Guyader F. S., Atmar R. L., Le Pendu J.. ( 2012; ). Transmission of viruses through shellfish: when specific ligands come into play. . Curr Opin Virol 2:, 103–110. [CrossRef] [PubMed]
    [Google Scholar]
  31. 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. [CrossRef] [PubMed]
    [Google Scholar]
  32. Lindesmith L., Moe C., Lependu J., Frelinger J. A., Treanor J., Baric R. S.. ( 2005; ). Cellular and humoral immunity following Snow Mountain virus challenge. . J Virol 79:, 2900–2909. [CrossRef] [PubMed]
    [Google Scholar]
  33. 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. [CrossRef] [PubMed]
    [Google Scholar]
  34. 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. [CrossRef] [PubMed]
    [Google Scholar]
  35. Makino A., Shimojima M., Miyazawa T., Kato K., Tohya Y., Akashi H.. ( 2006; ). Junctional adhesion molecule 1 is a functional receptor for feline calicivirus. . J Virol 80:, 4482–4490. [CrossRef] [PubMed]
    [Google Scholar]
  36. Ossiboff R. J., Sheh A., Shotton J., Pesavento P. A., Parker J. S.. ( 2007; ). Feline caliciviruses (FCVs) isolated from cats with virulent systemic disease possess in vitro phenotypes distinct from those of other FCV isolates. . J Gen Virol 88:, 506–517. [CrossRef] [PubMed]
    [Google Scholar]
  37. Ossiboff R. J., Zhou Y., Lightfoot P. J., Prasad B. V. V., Parker J. S. L.. ( 2010; ). Conformational changes in the capsid of a calicivirus upon interaction with its functional receptor. . J Virol 84:, 5550–5564. [CrossRef] [PubMed]
    [Google Scholar]
  38. Patel M. M., Widdowson M. A., Glass R. I., Akazawa K., Vinjé J., Parashar U. D.. ( 2008; ). Systematic literature review of role of noroviruses in sporadic gastroenteritis. . Emerg Infect Dis 14:, 1224–1231. [CrossRef] [PubMed]
    [Google Scholar]
  39. Richards G. P.. ( 2012; ). Critical review of norovirus surrogates in food safety research: rationale for considering volunteer studies. . Food Environ Virol 4:, 6–13. [CrossRef] [PubMed]
    [Google Scholar]
  40. 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. [CrossRef] [PubMed]
    [Google Scholar]
  41. 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. [CrossRef] [PubMed]
    [Google Scholar]
  42. Souza M., Azevedo M. S., Jung K., Cheetham S., Saif L. J.. ( 2008; ). Pathogenesis and immune responses in gnotobiotic calves after infection with the genogroup II.4-HS66 strain of human norovirus. . J Virol 82:, 1777–1786. [CrossRef] [PubMed]
    [Google Scholar]
  43. Souza F., Alfieri A. A., Alfieri A. F., Lorenzetti E., Headley S. A., Passos F., Silvestre T., Zago L., Mottin V. et al. ( 2012; ). The evaluation of enteric viruses in asymptomatic free-ranging non-human primates (Alouatta guariba clamitans, Alouatta caraya, Callithrix spp., Callithrix penicillata, and Leontopithecus caissara) in southern Brazil. . J Med Primatol 41:, 304–308. [CrossRef] [PubMed]
    [Google Scholar]
  44. Stuart A. D., Brown T. D.. ( 2007; ). α2,6-Linked sialic acid acts as a receptor for Feline calicivirus. . J Gen Virol 88:, 177–186. [CrossRef] [PubMed]
    [Google Scholar]
  45. Taube S., Kolawole A. O., Höhne M., Wilkinson J. E., Handley S. A., Perry J. W., Thackray L. B., Akkina R., Wobus C. E.. ( 2013; ). A mouse model for human norovirus. . MBio 4:, e00450-13. [CrossRef] [PubMed]
    [Google Scholar]
  46. Thackray L. B., Wobus C. E., Chachu K. A., Liu B., Alegre E. R., Henderson K. S., Kelley S. T., Virgin H. W. IV. ( 2007; ). Murine noroviruses comprising a single genogroup exhibit biological diversity despite limited sequence divergence. . J Virol 81:, 10460–10473. [CrossRef] [PubMed]
    [Google Scholar]
  47. Vashist S., Bailey D., Putics A., Goodfellow I.. ( 2009; ). Model systems for the study of human norovirus biology. . Future Virol 4:, 353–367. [CrossRef] [PubMed]
    [Google Scholar]
  48. Wang Q., Hirneisen K. A., Markland S. M., Kniel K. E.. ( 2013; ). Survival of murine norovirus, Tulane virus, and hepatitis A virus on alfalfa seeds and sprouts during storage and germination. . Appl Environ Microbiol 79:, 7021–7027. [CrossRef] [PubMed]
    [Google Scholar]
  49. Wei C., Farkas T., Sestak K., Jiang X.. ( 2008; ). Recovery of infectious virus by transfection of in vitro-generated RNA from Tulane calicivirus cDNA. . J Virol 82:, 11429–11436. [CrossRef] [PubMed]
    [Google Scholar]
  50. White L. J., Ball J. M., Hardy M. E., Tanaka T. N., Kitamoto N., Estes M. K.. ( 1996; ). Attachment and entry of recombinant Norwalk virus capsids to cultured human and animal cell lines. . J Virol 70:, 6589–6597.[PubMed]
    [Google Scholar]
  51. 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. [CrossRef] [PubMed]
    [Google Scholar]
  52. Zhang D., Huang P., Zou L., Lowary T. L., Tan M., Jiang X.. ( 2015; ). Tulane virus recognizes the A type 3 and B histo-blood group antigens. . J Virol 89:, 1419–1427. [CrossRef] [PubMed]
    [Google Scholar]
  53. 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. [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000020
Loading
/content/journal/jgv/10.1099/jgv.0.000020
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