Genetic and phenotypic characterization of GII-4 noroviruses that circulated during 1987 to 2008

Journal of Virology

Volumn 84, Issue 18, 2010, Pages 9595-9607

  Yang, Yang ^a,b   Xia, Ming ^b   Tan, Ming ^b   Huang, Pengwei ^b   Zhong, Weiming ^b   Pang, Xiao Li ^c   Lee, Bonita E ^c   Meller, Jarek ^b   Wang, Tao ^a   Jiang, Xi ^b  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD GROUP A ANTIGEN; BLOOD GROUP B ANTIGEN; BLOOD GROUP H ANTIGEN; BLOOD GROUP O ANTIGEN; OLIGOSACCHARIDE; SPHINGOLIPID ACTIVATOR PROTEIN 2; BLOOD GROUP ANTIGEN; VIRUS ANTIBODY; VIRUS RNA;

AMINO ACID SUBSTITUTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGENICITY; ARTICLE; BINDING AFFINITY; BINDING ASSAY; BINDING SITE; CROSS REACTION; ENZYME IMMUNOASSAY; GENE CLUSTER; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC VARIABILITY; GENOTYPE; HUMAN; IMMUNIZATION; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; NOROVIRUS; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; RECEPTOR BLOCKING; SALIVA ANALYSIS; SEQUENCE ANALYSIS; UNINDEXED SEQUENCE; VIRAL GENETICS; VIRUS CAPSID; VIRUS INFECTION; VIRUS STRAIN; WESTERN BLOTTING; ANIMAL; BAGG ALBINO MOUSE; CALICIVIRIDAE INFECTIONS; CANADA; CLUSTER ANALYSIS; DNA SEQUENCE; GASTROENTERITIS; GENETICS; IMMUNOLOGY; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR EVOLUTION; PATHOGENICITY; SALIVA; SEQUENCE HOMOLOGY; UNITED STATES; VIROLOGY; VIRUS ATTACHMENT;

ANIMALS; ANTIBODIES, VIRAL; BLOOD GROUP ANTIGENS; CALICIVIRIDAE INFECTIONS; CANADA; CLUSTER ANALYSIS; EVOLUTION, MOLECULAR; GASTROENTERITIS; GENOTYPE; HUMANS; MICE; MICE, INBRED BALB C; NOROVIRUS; OLIGOSACCHARIDES; RNA, VIRAL; SALIVA; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY; UNITED STATES; VIRUS ATTACHMENT;

EID: 77956031440     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02614-09     Document Type: Article

References (75)

1. Allen, D. J., J. J. Gray, C. I. Gallimore, J. Xerry, and M. Iturriza-Gomara. 2008. Analysis of amino acid variation in the P2 domain of the GII-4 norovirus VP1 protein reveals putative variant-specific epitopes. PLoS One 3:e1485.
2. Allen, D. J., R. Noad, D. Samuel, J. J. Gray, P. Roy, and M. Iturriza-Gomara. 2009. Characterisation of a GII-4 norovirus variant-specific surface-exposed site involved in antibody binding. Virol. J. 6:150.
3. Baric, R. S., B. Yount, L. Lindesmith, P. R. Harrington, S. R. Greene, F. C. Tseng, N. Davis, R. E. Johnston, D. G. Klapper, and C. L. Moe. 2002. Expression and self-assembly of Norwalk virus capsid protein from Venezuelan equine encephalitis virus replicons. J. Virol. 76:3023-3030.
4. Bok, K., E. J. Abente, M. Realpe-Quintero, T. Mitra, S. V. Sosnovtsev, A. Z. Kapikian, and K. Y. Green. 2009. Evolutionary dynamics of GII.4 noroviruses over a 34-year period. J. Virol. 83:11890-11901.
5. Bu, W., A. Mamedova, M. Tan, M. Xia, X. Jiang, and R. S. Hegde. 2008. Structural basis for the receptor binding specificity of Norwalk virus. J. Virol. 82:5340-5347.
6. Cannon, J. L., L. C. Lindesmith, E. F. Donaldson, L. Saxe, R. S. Baric, and J. Vinje. 2009. Herd immunity to GII.4 noroviruses is supported by outbreak patient sera. J. Virol. 83:5363-5374.
7. Cao, S., Z. Lou, M. Tan, Y. Chen, Y. Liu, Z. Zhang, X. C. Zhang, X. Jiang, X. Li, and Z. Rao. 2007. Structural basis for the recognition of blood group trisaccharides by norovirus. J. Virol. 81:5949-5957.
8. Castresana, J. 2000. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17:540-552.
9. Choi, J. M., A. M. Hutson, M. K. Estes, and B. V. Prasad. 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.
10. Dereeper, A., V. Guignon, G. Blanc, S. Audic, S. Buffet, F. Chevenet, J. F. Dufayard, S. Guindon, V. Lefort, M. Lescot, J. M. Claverie, and O. Gascuel. 2008. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 36:W465-W469.
11. Donaldson, E. F., L. C. Lindesmith, A. D. Lobue, and R. S. Baric. 2008. Norovirus pathogenesis: mechanisms of persistence and immune evasion in human populations. Immunol. Rev. 225:190-211.
12. Edgar, R. C. 2004. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113.
13. Fankhauser, R. L., S. S. Monroe, J. S. Noel, C. D. Humphrey, J. S. Bresee, U. D. Parashar, T. Ando, and R. I. Glass. 2002. Epidemiologic and molecular trends of "Norwalk-like viruses" associated with outbreaks of gastroenteritis in the United States. J. Infect. Dis. 186:1-7.
14. Felsenstein, J. 1989. PHYLIP - phylogeny inference package (version 3.2). Cladistics 5:164-166.
15. Franco, R. F., B. P. Simoes, and M. A. Zago. 1995. Relative frequencies of the two O alleles of the histo-blood ABH system in different racial groups. Vox Sang. 69:50-52.
16. Graham, D. Y., X. Jiang, T. Tanaka, A. R. Opekun, H. P. Madore, and M. K. Estes. 1994. Norwalk virus infection of volunteers: new insights based on improved assays. J. Infect. Dis. 170:34-43.
17. Green, K. Y., J. F. Lew, X. Jiang, A. Z. Kapikian, and M. K. Estes. 1993. Comparison of the reactivities of baculovirus-expressed recombinant Norwalk virus capsid antigen with those of the native Norwalk virus antigen in serologic assays and some epidemiologic observations. J. Clin. Microbiol. 31:2185-2191.
18. Guindon, S., and O. Gascuel. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52:696-704.
19. Harrington, P. R., L. Lindesmith, B. Yount, C. L. Moe, and R. S. Baric. 2002. Binding of Norwalk virus-like particles to ABH histo-blood group antigens is blocked by antisera from infected human volunteers or experimentally vaccinated mice. J. Virol. 76:12335-12343.
20. Harrington, P. R., J. Vinje, C. L. Moe, and R. S. Baric. 2004. Norovirus capture with histo-blood group antigens reveals novel virus-ligand interactions. J. Virol. 78:3035-3045.
21. Hein, J. 1990. Unified approach to alignment and phylogenies. Methods Enzymol. 183:626-645.
22. Holgersson, J., M. E. Breimer, and B. E. Samuelsson. 1992. Basic biochemistry of cell surface carbohydrates and aspects of the tissue distribution of histo-blood group ABH and related glycosphingolipids. APMIS Suppl. 27:18-27.
23. Huang, P., T. Farkas, S. Marionneau, W. Zhong, N. Ruvoen-Clouet, A. L. Morrow, M. Altaye, L. K. Pickering, D. S. Newburg, J. LePendu, and X. Jiang. 2003. Noroviruses bind to human ABO, Lewis, and secretor histo-blood group antigens: identification of 4 distinct strain-specific patterns. J. Infect. Dis. 188:19-31.
24. Huang, P., T. Farkas, W. Zhong, M. Tan, S. Thornton, A. L. Morrow, and X. Jiang. 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.
25. Hutson, A. M., F. Airaud, J. LePendu, M. K. Estes, and R. L. Atmar. 2005. Norwalk virus infection associates with secretor status genotyped from sera. J. Med. Virol. 77:116-120.
26. Hutson, A. M., R. L. Atmar, and M. K. Estes. 2004. Norovirus disease: changing epidemiology and host susceptibility factors. Trends Microbiol. 12:279-287.
27. Hutson, A. M., R. L. Atmar, D. Y. Graham, and M. K. Estes. 2002. Norwalk virus infection and disease is associated with ABO histo-blood group type. J. Infect. Dis. 185:1335-1337.
28. Hutson, A. M., R. L. Atmar, D. M. Marcus, and M. K. Estes. 2003. Norwalk virus-like particle hemagglutination by binding to H histo-blood group antigens. J. Virol. 77:405-415.
29. Jiang, X. 2003. Development of serological and molecular tests for the diagnosis of calicivirus infections, p. 505-522. In U. Desselberger and J. Gray (ed.), Viral gastroenteritis, 1st ed. Elsevier Science B. V., Amsterdam, Netherlands.
30. Jiang, X., D. Cubitt, J. Hu, X. Dai, J. Treanor, D. O. Matson, and L. K. Pickering. 1995. Development of an ELISA to detect MX virus, a human calicivirus in the Snow Mountain agent genogroup. J. Gen. Virol. 76(11):2739-2747.
31. Jiang, X., D. O. Matson, G. M. Ruiz-Palacios, J. Hu, J. Treanor, and L. K. Pickering. 1995. Expression, self-assembly, and antigenicity of a snow mountain agent-like calicivirus capsid protein. J. Clin. Microbiol. 33:1452-1455.
32. Jiang, X., M. Wang, D. Y. Graham, and M. K. Estes. 1992. Expression, self-assembly, and antigenicity of the Norwalk virus capsid protein. J. Virol. 66:6527-6532.
33. Jiang, X., M. Wang, K. Wang, and M. K. Estes. 1993. Sequence and genomic organization of Norwalk virus. Virology 195:51-61.
34. Jiang, X., N. Wilton, W. M. Zhong, T. Farkas, P. W. Huang, E. Barrett, M. Guerrero, G. Ruiz-Palacios, K. Y. Green, J. Green, A. D. Hale, M. K. Estes, L. K. Pickering, and D. O. Matson. 2000. Diagnosis of human caliciviruses by use of enzyme immunoassays. J. Infect. Dis. 181(Suppl. 2):S349-S359.
35. Jin, M., H. P. Xie, Z. J. Duan, N. Liu, Q. Zhang, B. S. Wu, H. Y. Li, W. X. Cheng, S. H. Yang, J. M. Yu, Z. Q. Xu, S. X. Cui, L. Zhu, M. Tan, X. Jiang, and Z. Y. Fang. 2008. Emergence of the GII4/2006b variant and recombinant noroviruses in China. J. Med. Virol. 80:1997-2004.
36. Lambden, P. R., E. O. Caul, C. R. Ashley, and I. N. Clarke. 1993. Sequence and genome organization of a human small round-structured (Norwalk-like) virus. Science 259:516-519.
37. Larkin, M. A., G. Blackshields, N. P. Brown, R. Chenna, P. A. McGettigan, H. McWilliam, F. Valentin, I. M. Wallace, A. Wilm, R. Lopez, J. D. Thompson, T. J. Gibson, and D. G. Higgins. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948.
38. Le, S. Q., and O. Gascuel. 2008. An improved general amino acid replacement matrix. Mol. Biol. Evol. 25:1307-1320.
39. Lee, B. E., J. K. Preiksaitis, N. Chui, L. Chui, and X. L. Pang. 2008. Genetic relatedness of noroviruses identified in sporadic gastroenteritis in children and gastroenteritis outbreaks in northern Alberta. J. Med. Virol. 80:330-337.
40. Le Pendu, J. 2004. Histo-blood group antigen and human milk oligosaccharides: genetic polymorphism and risk of infectious diseases. Adv. Exp. Med. Biol. 554:135-143.
41. Lindesmith, L., C. Moe, J. Lependu, J. A. Frelinger, J. Treanor, and R. S. Baric. 2005. Cellular and humoral immunity following Snow Mountain virus challenge. J. Virol. 79:2900-2909.
42. Lindesmith, L., C. Moe, S. Marionneau, N. Ruvoen, X. Jiang, L. Lindblad, P. Stewart, J. LePendu, and R. Baric. 2003. Human susceptibility and resistance to Norwalk virus infection. Nat. Med. 9:548-553.
43. Lindesmith, L. C., E. F. Donaldson, A. D. Lobue, J. L. Cannon, D. P. Zheng, J. Vinje, and R. S. Baric. 2008. Mechanisms of GII.4 norovirus persistence in human populations. PLoS Med. 5:e31.
44. Lopman, B. A., M. H. Reacher, Y. Van Duijnhoven, F. X. Hanon, D. Brown, and M. Koopmans. 2003. Viral gastroenteritis outbreaks in Europe, 1995-2000. Emerg. Infect. Dis. 9:90-96.
45. Marionneau, S., N. Ruvoen, B. Le Moullac-Vaidye, M. Clement, A. Cailleau- Thomas, G. Ruiz-Palacois, P. Huang, X. Jiang, and J. Le Pendu. 2002. Norwalk virus binds to histo-blood group antigens present on gastroduodenal epithelial cells of secretor individuals. Gastroenterology 122:1967-1977. (Pubitemid 34651439)
46. Monroe, S. S., S. E. Stine, X. Jiang, M. K. Estes, and R. I. Glass. 1993. Detection of antibody to recombinant Norwalk virus antigen in specimens from outbreaks of gastroenteritis. J. Clin. Microbiol. 31:2866-2872.
47. Néron, B., H. Menager, C. Maufrais, N. Joly, J. Maupetit, S. Letort, S. Carrere, P. Tuffery, and C. Letondal. 2009. Mobyle: a new full web bioinformatics framework. Bioinformatics 25:3005-3011.
48. Nguyen, T. A., F. Yagyu, M. Okame, T. G. Phan, Q. D. Trinh, H. Yan, K. T. Hoang, A. T. Cao, P. Le Hoang, S. Okitsu, and H. Ushijima. 2007. Diversity of viruses associated with acute gastroenteritis in children hospitalized with diarrhea in Ho Chi Minh City, Vietnam. J. Med. Virol. 79:582-590.
49. Noel, J. S., R. L. Fankhauser, T. Ando, S. S. Monroe, and R. I. Glass. 1999. Identification of a distinct common strain of "Norwalk-like viruses" having a global distribution. J. Infect. Dis. 179:1334-1344.
50. Nordgren, J., E. Kindberg, P. E. Lindgren, A. Matussek, and L. Svensson. 2010. Norovirus gastroenteritis outbreak with a secretor-independent susceptibility pattern, Sweden. Emerg. Infect. Dis. 16:81-87.
51. Parker, S., D. Cubitt, J. X. Jiang, and M. Estes. 1993. Efficacy of a recombinant Norwalk virus protein enzyme immunoassay for the diagnosis of infections with Norwalk virus and other human "candidate" caliciviruses. J. Med. Virol. 41:179-184.
52. Prasad, B. V., M. E. Hardy, T. Dokland, J. Bella, M. G. Rossmann, and M. K. Estes. 1999. X-ray crystallographic structure of the Norwalk virus capsid. Science 286:287-290.
53. Rockx, B. H., H. Vennema, C. J. Hoebe, E. Duizer, and M. P. Koopmans. 2005. Association of histo-blood group antigens and susceptibility to norovirus infections. J. Infect. Dis. 191:749-754.
54. Seto, Y., N. Iritani, H. Kubo, A. Kaida, T. Murakami, K. Haruki, O. Nishio, M. Ayata, and H. Ogura. 2005. Genotyping of norovirus strains detected in outbreaks between April 2002 and March 2003 in Osaka City, Japan. Microbiol. Immunol. 49:275-283.
55. Shirato, H., S. Ogawa, H. Ito, T. Sato, A. Kameyama, H. Narimatsu, Z. Xiaofan, T. Miyamura, T. Wakita, K. Ishii, and N. Takeda. 2008. Noroviruses distinguish between type 1 and type 2 histo-blood group antigens for binding. J. Virol. 82:10756-10767.
56. Siebenga, J. J., H. Vennema, B. Renckens, E. de Bruin, B. van der Veer, R. J. Siezen, and M. Koopmans. 2007. Epochal evolution of GGII.4 norovirus capsid proteins from 1995 to 2006. J. Virol. 81:9932-9941.
57. Siebenga, J. J., H. Vennema, D. P. Zheng, J. Vinje, B. E. Lee, X. L. Pang, E. C. Ho, W. Lim, A. Choudekar, S. Broor, T. Halperin, N. B. Rasool, J. Hewitt, G. E. Greening, M. Jin, Z. J. Duan, Y. Lucero, M. O'Ryan, M. Hoehne, E. Schreier, R. M. Ratcliff, P. A. White, N. Iritani, G. Reuter, and M. Koopmans. 2009. Norovirus illness is a global problem: emergence and spread of norovirus GII.4 variants, 2001-2007. J. Infect. Dis. 200:802-812.
58. Strimmer, K., and A. von Haeseler. 1997. Likelihood-mapping: a simple method to visualize phylogenetic content of a sequence alignment. Proc. Natl. Acad. Sci. U. S. A. 94:6815-6819.
59. Tan, M., P. Fang, T. Chachiyo, M. Xia, P. Huang, Z. Fang, W. Jiang, and X. Jiang. 2008. Noroviral P particle: structure, function and applications in virus-host interaction. Virology 382:115-123.
60. Tan, M., R. S. Hegde, and X. Jiang. 2004. The P domain of norovirus capsid protein forms dimer and binds to histo-blood group antigen receptors. J. Virol. 78:6233-6242.
61. Tan, M., P. Huang, J. Meller, W. Zhong, T. Farkas, and X. Jiang. 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. (Pubitemid 37430652)
62. Tan, M., and X. Jiang. 2008. Association of histo-blood group antigens with susceptibility to norovirus infection may be strain-specific rather than genogroup dependent. J. Infect. Dis. 198:940-941.
63. Tan, M., and X. Jiang. 2007. Norovirus-host interaction: implications for disease control and prevention. Expert Rev. Mol. Med. 9:1-22.
64. Tan, M., and X. Jiang. 2005. Norovirus and its histo-blood group antigen receptors: an answer to a historical puzzle. Trends Microbiol. 13:285-293.
65. Tan, M., and X. Jiang. 2005. The P domain of norovirus capsid protein forms a subviral particle that binds to histo-blood group antigen receptors. J. Virol. 79:14017-14030.
66. Tan, M., M. Jin, H. Xie, Z. Duan, X. Jiang, and Z. Fang. 2008. Outbreak studies of a GII-3 and a GII-4 norovirus revealed an association between HBGA phenotypes and viral infection. J. Med. Virol. 80:1296-1301.
67. Tan, M., J. Meller, and X. Jiang. 2006. C-terminal arginine cluster is essential for receptor binding of norovirus capsid protein. J. Virol. 80:7322-7331.
68. Tan, M., M. Xia, S. Cao, P. Huang, T. Farkas, J. Meller, R. S. Hegde, X. Li, Z. Rao, and X. Jiang. 2008. Elucidation of strain-specific interaction of a GII-4 norovirus with HBGA receptors by site-directed mutagenesis study. Virology 379:324-334.
69. Tan, M., M. Xia, Y. Chen, W. Bu, R. S. Hegde, J. Meller, X. Li, and X. Jiang. 2009. Conservation of carbohydrate binding interfaces: evidence of human HBGA selection in norovirus evolution. PLoS One 4:e5058.
70. Tan, M., W. Zhong, D. Song, S. Thornton, and X. Jiang. 2004. E. coli-expressed recombinant norovirus capsid proteins maintain authentic antigenicity and receptor binding capability. J. Med. Virol. 74:641-649.
71. Victoria, M., M. P. Miagostovich, M. S. Ferreira, C. B. Vieira, J. M. Fioretti, J. P. Leite, R. Colina, and J. Cristina. 2009. Bayesian coalescent inference reveals high evolutionary rates and expansion of norovirus populations. Infect. Genet. Evol. 9:927-932.
72. Xerry, J., C. I. Gallimore, M. Iturriza-Gomara, D. J. Allen, and J. J. Gray. 2008. Transmission events within outbreaks of gastroenteritis determined through analysis of nucleotide sequences of the P2 domain of genogroup II noroviruses. J. Clin. Microbiol. 46:947-953.
73. Xi, J. N., D. Y. Graham, K. N. Wang, and M. K. Estes. 1990. Norwalk virus genome cloning and characterization. Science 250:1580-1583.
74. Zhao, Y. F., H. P. Xie1, H. X. Lv, Q. Zhang, M. Jin, Z. J. Duncan, D. Steele, B. M. Jiang, and X. Jiang. 2007. Investigation of human calicivirus (HuCV) diarrhea among infantile and young children in China, 1999-2005. Chin. J. Virol. 23:9-15.
75. Zheng, D. P., T. Ando, R. L. Fankhauser, R. S. Beard, R. I. Glass, and S. S. Monroe. 2006. Norovirus classification and proposed strain nomenclature. Virology 346:312-323.