A Unique Human Norovirus Lineage with a Distinct HBGA Binding Interface

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Human norovirus (huNoV) has diverged into two major lineages (GI and GII) selected by the host histo-blood group antigens (HBGAs). Both lineages further diverge into various sub-lineages (genotypes) that recognize different ABH and Lewis antigens through a common HBGA binding interface shared among strains within each genogroup. In this study, through X-ray crystallography of the P domain of a GII.21 huNoV (OIF) we identified a unique lineage in GII consisting of GII.13 and GII.21 genotypes that recognize HBGAs through a binding interface distinct from the GII conventional binding interface. While the mechanism remains unknown, our finding raises an alert on future emergence of new lineages by the same way via developing new receptor binding interfaces, as well as further divergence of this new lineage into more sub-lineages recognizing different HBGAs, which may impact future epidemiology and strategies for disease control and prevention against huNoVs.

Vyšlo v časopise: A Unique Human Norovirus Lineage with a Distinct HBGA Binding Interface. PLoS Pathog 11(7): e32767. doi:10.1371/journal.ppat.1005025
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1005025

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1. Payne DC, Vinje J, Szilagyi PG, Edwards KM, Staat MA, Weinberg GA, et al. Norovirus and medically attended gastroenteritis in U.S. children. The New England journal of medicine. 2013;368(12):1121–30. doi: 10.1056/NEJMsa1206589 23514289.

2. Patel MM, Widdowson MA, Glass RI, Akazawa K, Vinje J, Parashar UD. Systematic literature review of role of noroviruses in sporadic gastroenteritis. Emerg Infect Dis. 2008;14(8):1224–31. Epub 2008/08/06. 18680645. doi: 10.3201/eid1408.071114

3. Prasad BV, Hardy ME, Dokland T, Bella J, Rossmann MG, Estes MK. X-ray crystallographic structure of the Norwalk virus capsid. Science. 1999;286(5438):287–90. 10514371.

4. Huang P, Farkas T, Marionneau S, Zhong W, Ruvoen-Clouet N, Morrow AL, et al. Noroviruses Bind to Human ABO, Lewis, and Secretor Histo-Blood Group Antigens: Identification of 4 Distinct Strain-Specific Patterns. J Infect Dis. 2003;188(1):19–31. 12825167.

5. Huang P, Farkas T, Zhong W, Tan M, Thornton S, Morrow AL, et al. 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. 2005;79(11):6714–22. Epub 2005/05/14. doi: 79/11/6714 [pii] doi: 10.1128/JVI.79.11.6714–6722.2005 15890909; PubMed Central PMCID: PMC1112114.

6. Ravn V, Dabelsteen E. Tissue distribution of histo‐blood group antigens. Apmis. 2000;108(1):1–28. 10698081

7. Frenck R, Bernstein DI, Xia M, Huang P, Zhong W, Parker S, et al. Predicting Susceptibility to Norovirus GII.4 by Use of a Challenge Model Involving Humans. J Infect Dis. 2012;206(9):1386–93. doi: 10.1093/infdis/jis514 22927452.

8. Hutson AM, Atmar RL, Graham DY, Estes MK. Norwalk virus infection and disease is associated with ABO histo-blood group type. J Infect Dis. 2002;185(9):1335–7. 12001052.

9. Lindesmith L, Moe C, Marionneau S, Ruvoen N, Jiang X, Lindblad L, et al. Human susceptibility and resistance to Norwalk virus infection. Nat Med. 2003;9(5):548–53. 12692541.

10. Tan M, Jin M, Xie H, Duan Z, Jiang X, Fang Z. Outbreak studies of a GII-3 and a GII-4 norovirus revealed an association between HBGA phenotypes and viral infection. Journal of medical virology. 2008;80(7):1296–301. 18461617. doi: 10.1002/jmv.21200

11. Nordgren J, Nitiema LW, Ouermi D, Simpore J, Svensson L. Host genetic factors affect susceptibility to norovirus infections in Burkina Faso. PLoS One. 2013;8(7):e69557. doi: 10.1371/journal.pone.0069557 23894502; PubMed Central PMCID: PMC3716642.

12. Jones MK, Watanabe M, Zhu S, Graves CL, Keyes LR, Grau KR, et al. Enteric bacteria promote human and mouse norovirus infection of B cells. Science. 2014;346(6210):755–9. doi: 10.1126/science.1257147 25378626.

13. Katayama K, Murakami K, Sharp TM, Guix S, Oka T, Takai-Todaka R, et al. Plasmid-based human norovirus reverse genetics system produces reporter-tagged progeny virus containing infectious genomic RNA. Proceedings of the National Academy of Sciences of the United States of America. 2014;111(38):E4043–52. doi: 10.1073/pnas.1415096111 25192933; PubMed Central PMCID: PMC4183323.

14. Taube S, Kolawole AO, Hohne M, Wilkinson JE, Handley SA, Perry JW, et al. A mouse model for human norovirus. mBio. 2013;4(4):e00450–13. doi: 10.1128/mBio.00450-13 23860770; PubMed Central PMCID: PMC3735125.

15. Tan M, Hegde RS, Jiang X. The P domain of norovirus capsid protein forms dimer and binds to histo-blood group antigen receptors. J Virol. 2004;78(12):6233–42. 15163716.

16. Tan M, Fang PA, Xia M, Chachiyo T, Jiang W, Jiang X. Terminal modifications of norovirus P domain resulted in a new type of subviral particles, the small P particles. Virology. 2011;410(2):345–52. Epub 2010/12/28. doi: S0042-6822(10)00735-X [pii] doi: 10.1016/j.virol.2010.11.017 21185050; PubMed Central PMCID: PMC3064930.

17. Tan M, Fang P, Chachiyo T, Xia M, Huang P, Fang Z, et al. Noroviral P particle: structure, function and applications in virus-host interaction. Virology. 2008;382(1):115–23. 18926552. doi: 10.1016/j.virol.2008.08.047

18. Tan M, Jiang X. The p domain of norovirus capsid protein forms a subviral particle that binds to histo-blood group antigen receptors. J Virol. 2005;79(22):14017–30. 16254337.

19. Bu W, Mamedova A, Tan M, Xia M, Jiang X, Hegde RS. Structural basis for the receptor binding specificity of Norwalk virus. J Virol. 2008;82(11):5340–7. Epub 2008/04/04. doi: JVI.00135-08 [pii] doi: 10.1128/JVI.00135-08 18385236.

20. Cao S, Lou Z, Tan M, Chen Y, Liu Y, Zhang Z, et al. Structural basis for the recognition of blood group trisaccharides by norovirus. J Virol. 2007;81(11):5949–57. Epub 2007/03/30. doi: JVI.00219-07 [pii] doi: 10.1128/JVI.00219-07 17392366; PubMed Central PMCID: PMC1900264.

21. Chen Y, Tan M, Xia M, Hao N, Zhang XC, Huang P, et al. Crystallography of a lewis-binding norovirus, elucidation of strain-specificity to the polymorphic human histo-blood group antigens. PLoS pathogens. 2011;7(7):e1002152. Epub 2011/08/04. doi: 10.1371/journal.ppat.1002152 PPATHOGENS-D-10-00601 [pii]. 21811409; PubMed Central PMCID: PMC3141052.

22. Choi JM, Hutson AM, Estes MK, Prasad BV. Atomic resolution structural characterization of recognition of histo-blood group antigens by Norwalk virus. Proceedings of the National Academy of Sciences of the United States of America. 2008;105(27):9175–80. Epub 2008/07/05. doi: 0803275105 [pii] doi: 10.1073/pnas.0803275105 18599458.

23. Hansman GS, Biertumpfel C, Georgiev I, McLellan JS, Chen L, Zhou T, et al. Crystal Structures of GII.10 and GII.12 Norovirus Protruding Domains in Complex with Histo-Blood Group Antigens Reveal Details for a Potential Site of Vulnerability. J Virol. 2011;85(13):6687–701. Epub 2011/04/29. doi: JVI.00246-11 [pii] doi: 10.1128/JVI.00246-11 21525337.

24. Kubota T, Kumagai A, Ito H, Furukawa S, Someya Y, Takeda N, et al. Structural basis for the recognition of Lewis antigens by genogroup I norovirus. J Virol. 2012;86(20):11138–50. doi: 10.1128/JVI.00278-12 22855491; PubMed Central PMCID: PMC3457155.

25. Shanker S, Czako R, Sankaran B, Atmar RL, Estes MK, Prasad BV. Structural analysis of determinants of histo-blood group antigen binding specificity in genogroup I noroviruses. J Virol. 2014;88(11):6168–80. doi: 10.1128/JVI.00201-14 24648450; PubMed Central PMCID: PMC4093872.

26. Hao H, Chen Y, Xia M, Tan M, Liu W, Guan X, et al. Crystal structures of GI.8 Boxer P dimers in complex with HBGAs, a novel evolutionary path selected by the Lewis epitope. Protein and Cell. 2014;in press.

27. Tan M, Jiang X. Norovirus gastroenteritis, carbohydrate receptors, and animal models. PLoS pathogens. 2010;6(8):e1000983. Epub 2010/09/25. doi: 10.1371/journal.ppat.1000983 20865168; PubMed Central PMCID: PMC2928792.

28. Tan M, Jiang X. Norovirus-host interaction: Multi-selections by human histo-blood group antigens. Trends in microbiology. 2011;19(8):382–8. Epub 2011/06/28. doi: S0966-842X(11)00108-9 [pii] doi: 10.1016/j.tim.2011.05.007 21705222; PubMed Central PMCID: PMC3149758.

29. Tan M, Jiang X. Histo-blood group antigens: a common niche for norovirus and rotavirus. Expert Rev Mol Med. 2014;16:e5. doi: 10.1017/erm.2014.2 24606759.

30. Tan M, Zhong W, Song D, Thornton S, Jiang X. E. coli-expressed recombinant norovirus capsid proteins maintain authentic antigenicity and receptor binding capability. Journal of medical virology. 2004;74(4):641–9. 15484274.

31. Tan M, Xia M, Chen Y, Bu W, Hegde RS, Meller J, et al. Conservation of carbohydrate binding interfaces: evidence of human HBGA selection in norovirus evolution. PLoS One. 2009;4(4):e5058. Epub 2009/04/02. doi: 10.1371/journal.pone.0005058 19337380; PubMed Central PMCID: PMC2660415.

32. Chen YT, Tan M, Xia M, Hao N, Zhang XJC, Huang PW, et al. Crystallography of a Lewis-Binding Norovirus, Elucidation of Strain-Specificity to the Polymorphic Human Histo-Blood Group Antigens. Plos Pathogens. 2011;7(7). doi: e100215210.1371/journal.ppat.1002152. WOS:000293339300040.

33. Tan M, Xia M, Cao S, Huang P, Farkas T, Meller J, et al. Elucidation of strain-specific interaction of a GII-4 norovirus with HBGA receptors by site-directed mutagenesis study. Virology. 2008;379(2):324–34. doi: 10.1016/j.virol.2008.06.041 18692213

34. de Rougemont A, Ruvoen-Clouet N, Simon B, Estienney M, Elie-Caille C, Aho S, et al. Qualitative and quantitative analysis of the binding of GII.4 norovirus variants onto human blood group antigens. J Virol. 2011;85(9):4057–70. Epub 2011/02/25. doi: JVI.02077-10 [pii] doi: 10.1128/JVI.02077-10 21345963; PubMed Central PMCID: PMC3126233.

35. Lindesmith LC, Donaldson EF, Lobue AD, Cannon JL, Zheng DP, Vinje J, et al. Mechanisms of GII.4 norovirus persistence in human populations. PLoS Med. 2008;5(2):e31. 18271619. doi: 10.1371/journal.pmed.0050031

36. Jin M, Tan M, Xia M, Wei C, Huang P, Wang L, et al. Strain-specific interaction of a GII.10 Norovirus with HBGAs. Virology. 2015;476 : 386–94. doi: 10.1016/j.virol.2014.12.039 25591173.

37. Hoa-Tran TN, Nakagomi T, Sano D, Sherchand JB, Pandey BD, Cunliffe NA, et al. Molecular epidemiology of noroviruses detected in Nepalese children with acute diarrhea between 2005 and 2011: increase and predominance of minor genotype GII.13. Infection, genetics and evolution: journal of molecular epidemiology and evolutionary genetics in infectious diseases. 2015;30 : 27–36. doi: 10.1016/j.meegid.2014.12.003 25497351.

38. Shirato H, Ogawa S, Ito H, Sato T, Kameyama A, Narimatsu H, et al. Noroviruses Distinguish between Type 1 and Type 2 Histo-Blood Group Antigens for Binding. J Virol. 2008;82(21):10756–67. doi: 10.1128/JVI.00802-08 18701592

39. Yahiro T, Wangchuk S, Wada T, Dorji C, Matsumoto T, Mynak ML, et al. Norovirus GII.21 in Children with Diarrhea, Bhutan. Emerg Infect Dis. 2015;21(4):732–4. doi: 10.3201/eid2104.141856 25811105; PubMed Central PMCID: PMC4378497.

40. Bruggink LD, Dunbar NL, Marshall JA. Norovirus genotype diversity associated with gastroenteritis outbreaks in aged-care facilities. Epidemiology and infection. 2015 : 1–5. doi: 10.1017/S095026881500031X 25721658.

41. Jing L, Limei S, Lin F, Feng Y, Yanling M, Jiaqian L, et al. Gastroenteritis Outbreaks Caused by Norovirus GII.17, Guangdong Province, China, 2014–2015. Emerging Infectious Disease journal. 2015;21(7). doi: 10.3201/eid2107.150226

42. Hansman GS, Shahzad-Ul-Hussan S, McLellan JS, Chuang GY, Georgiev I, Shimoike T, et al. Structural basis for norovirus inhibition and fucose mimicry by citrate. J Virol. 2012;86(1):284–92. doi: 10.1128/JVI.05909-11 22031945; PubMed Central PMCID: PMC3255897.

43. Otwinowski Z, Minor W. Processing of X-ray diffraction data collected in oscillation mode. Method Enzymol. 1997;276 : 307–26. doi: 10.1016/S0076-6879(97)76066-X WOS:A1997BH42P00020.

44. Bailey S. The Ccp4 Suite—Programs for Protein Crystallography. Acta Crystallogr D. 1994;50 : 760–3. WOS:A1994PK56800011.

45. Adams PD, Grosse-Kunstleve RW, Hung LW, Ioerger TR, McCoy AJ, Moriarty NW, et al. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr D. 2002;58 : 1948–54. doi: 10.1107/S0907444902016657 WOS:000178745000009.

46. Emsley P, Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr D. 2004;60 : 2126–32. doi: 10.1107/S0907444904019158 WOS:000225360500002.

47. Laskowski RA, MacArthur MW, Moss DS, Thornton JM. PROCHECK: a program to check the stereochemical quality of protein structures. Journal of Applied Crystallography. 1993;26(2):283–91.

48. Zhang XJ, Matthews BW. EDPDB: a multifunctional tool for protein structure analysis. Journal of Applied Crystallography. 1995;28(5):624–30.

49. DeLano WL. The PyMOL molecular graphics system. 2002.

50. Tan M, Fang P, Chachiyo T, Xia M, Huang P, Fang Z, et al. Noroviral P particle: Structure, function and applications in virus-host interaction. Virology. 2008;382 : 115–23. Epub 2008/10/18. doi: S0042-6822(08)00579-5 [pii] doi: 10.1016/j.virol.2008.08.047 18926552.

51. Tan M, Jiang X. The p domain of norovirus capsid protein forms a subviral particle that binds to histo-blood group antigen receptors. Journal of Virology. 2005;79(22):14017–30. 16254337.

52. Kroneman A, Vega E, Vennema H, Vinje J, White PA, Hansman G, et al. Proposal for a unified norovirus nomenclature and genotyping. Archives of virology. 2013;158(10):2059–68. doi: 10.1007/s00705-013-1708-5 23615870.