Home LiteratureArticle Details
PMID: 17652401 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Murine noroviruses comprising a single genogroup exhibit biological diversity despite limited sequence divergence.

Journal of virology ·Vol. 81 ·No. 19 ·2007-10-00 ·Pages 10460-73

Thackray LB, Wobus CE, Chachu KA, Liu B, Alegre ER, Henderson KS, Kelley ST, Virgin HW

Abstract

Viruses within the genus Norovirus of the family Caliciviridae are the major cause of acute, nonbacterial gastroenteritis worldwide. Human noroviruses are genetically diverse, with up to 57% divergence in capsid protein sequences, and comprise three genogroups. The significance of such genetic diversity is not yet understood. The discovery of murine norovirus (MNV) and its ability to productively infect cultured murine macrophages and dendritic cells has provided an opportunity to determine the functional consequences of norovirus diversity in vitro and in vivo. Therefore, we compared the full-length genomes of 21 new MNV isolates with five previously sequenced MNV genomes and demonstrated a conserved genomic organization consisting of four open reading frames (ORFs) and a previously unknown region of nucleotide conservation in ORF2. A phylogenetic analysis of all 26 MNV genomes revealed 15 distinct MNV strains, with up to 13% divergence at the nucleotide level, that comprise a single genotype and genogroup. Evidence for recombination within ORF2 in several MNV genomes was detected by multiple methods. Serological analyses comparing neutralizing antibody responses between highly divergent strains suggested that the MNV genogroup comprises a single serotype. Within this single genogroup, MNV strains exhibited considerable biological diversity in their ability to grow in culture and to infect and/or persist in wild-type mice. The isolation and characterization of multiple MNV strains illustrate how genetic analysis may underestimate the biological diversity of noroviruses and provide a molecular map for future studies of MNV biology.

MeSH Terms
Animals Antibodies, Viral/immunology Base Sequence Caliciviridae Infections/veterinary,virology Genetic Variation Genome/genetics Mice/virology Mice, Inbred Strains Molecular Sequence Data Neutralization Tests Norovirus/classification,genetics,isolation & purification Open Reading Frames Phylogeny Recombination, Genetic STAT1 Transcription Factor/genetics Sequence Analysis, DNA Serotyping
Chemicals
Antibodies, Viral STAT1 Transcription Factor Stat1 protein, mouse
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Thackray Larissa B
Department of Pathology and Immunology, Box 8118, Washington University School of Medicine, 660 S. Euclid Ave., St. Louis, MO 63110, USA.
Wobus Christiane E
Chachu Karen A
Liu Bo
Alegre Eric R
Henderson Kenneth S
Kelley Scott T
Virgin Herbert W
References (80)
80 references, click to expand
  1. Development of a microsphere-based serologic multiplexed fluorescent immunoassay and a reverse transcriptase PCR assay to detect murine norovirus 1 infection in mice.
    Clin Diagn Lab Immunol. 2005 Oct;12(10):1145-51 PMID: 16210475
  2. Molecular and epidemiologic trends of caliciviruses associated with outbreaks of acute gastroenteritis in the United States, 2000-2004.
    J Infect Dis. 2006 Feb 1;193(3):413-21 PMID: 16388489
  3. High throughput sequence analysis reveals hitherto unreported recombination in the genus Norovirus.
    Virology. 2006 Feb 5;345(1):88-95 PMID: 16263150
  4. Coexistence of multiple genotypes, including newly identified genotypes, in outbreaks of gastroenteritis due to Norovirus in Japan.
    J Clin Microbiol. 2004 Jul;42(7):2988-95 PMID: 15243049
  5. Mutation in a Lordsdale norovirus epidemic strain as a potential indicator of transmission routes.
    J Clin Microbiol. 2004 Sep;42(9):3950-7 PMID: 15364974
  6. Epidemiology and cost of nosocomial gastroenteritis, Avon, England, 2002-2003.
    Emerg Infect Dis. 2004 Oct;10(10):1827-34 PMID: 15504271
  7. Transmission of acute infectious nonbacterial gastroenteritis to volunteers by oral administration of stool filtrates.
    J Infect Dis. 1971 Mar;123(3):307-12 PMID: 5111887
  8. Comparison of three agents of acute infectious nonbacterial gastroenteritis by cross-challenge in volunteers.
    J Infect Dis. 1974 Jun;129(6):709-14 PMID: 4209723
  9. Solid-phase immune electron microscopy with human immunoglobulin M for serotyping of Norwalk-like viruses.
    J Clin Microbiol. 1988 May;26(5):938-42 PMID: 2838506
  10. Three serotypes of Norwalk-like virus demonstrated by solid-phase immune electron microscopy.
    J Med Virol. 1990 Jan;30(1):77-81 PMID: 2154547
  11. Intraluminal proteolytic activation plays an important role in replication of type 1 reovirus in the intestines of neonatal mice.
    J Virol. 1990 Apr;64(4):1830-3 PMID: 2157065
  12. Norwalk virus genome cloning and characterization.
    Science. 1990 Dec 14;250(4987):1580-3 PMID: 2177224
  13. Antigenic relatedness among the Norwalk-like agents by serum antibody rises.
    J Med Virol. 1990 Oct;32(2):96-101 PMID: 1704048
  14. Norwalk virus infection of volunteers: new insights based on improved assays.
    J Infect Dis. 1994 Jul;170(1):34-43 PMID: 8014518
  15. Estimating the pattern of nucleotide substitution.
    J Mol Evol. 1994 Jul;39(1):105-11 PMID: 8064867
  16. Antigenic mapping of the recombinant Norwalk virus capsid protein using monoclonal antibodies.
    Virology. 1996 Mar 1;217(1):252-61 PMID: 8599210
  17. Emergence of a new norovirus genotype II.4 variant associated with global outbreaks of gastroenteritis.
    J Clin Microbiol. 2006 Feb;44(2):327-33 PMID: 16455879
  18. Risk groups for clinical complications of norovirus infections: an outbreak investigation.
    Clin Microbiol Infect. 2006 Jan;12(1):69-74 PMID: 16460549
  19. Genetic and antigenic diversity among noroviruses.
    J Gen Virol. 2006 Apr;87(Pt 4):909-19 PMID: 16528040
  20. Norovirus classification and proposed strain nomenclature.
    Virology. 2006 Mar 15;346(2):312-23 PMID: 16343580
  21. Murine norovirus: a model system to study norovirus biology and pathogenesis.
    J Virol. 2006 Jun;80(11):5104-12 PMID: 16698991
  22. Changing distribution of norovirus genotypes and genetic analysis of recombinant GIIb among infants and children with diarrhea in Japan.
    J Med Virol. 2006 Jul;78(7):971-8 PMID: 16721850
  23. Viral gastroenteritis and genetic characterization of recombinant norovirus circulating in Eastern Russia.
    Clin Lab. 2006;52(5-6):247-53 PMID: 16812951
  24. Cleavage map and proteolytic processing of the murine norovirus nonstructural polyprotein in infected cells.
    J Virol. 2006 Aug;80(16):7816-31 PMID: 16873239
  25. Persistent infection with and serologic cross-reactivity of three novel murine noroviruses.
    Comp Med. 2006 Aug;56(4):247-51 PMID: 16941951
  26. Molecular epidemiology of norovirus infections in sporadic cases of viral gastroenteritis among children in Northern Italy.
    J Med Virol. 2006 Nov;78(11):1486-92 PMID: 16998898
  27. Genetic diversity of norovirus among children with gastroenteritis in São Paulo State, Brazil.
    J Clin Microbiol. 2006 Nov;44(11):3947-53 PMID: 16943348
  28. Prolonged norovirus shedding in infants <or=6 months of age with gastroenteritis.
    Pediatr Infect Dis J. 2007 Jan;26(1):46-9 PMID: 17195705
  29. Molecular characterization of three novel murine noroviruses.
    Virus Genes. 2007 Apr;34(2):147-55 PMID: 17171545
  30. Murine norovirus 1 infection is associated with histopathological changes in immunocompetent hosts, but clinical disease is prevented by STAT1-dependent interferon responses.
    J Virol. 2007 Apr;81(7):3251-63 PMID: 17229692
  31. Recovery of infectious murine norovirus using pol II-driven expression of full-length cDNA.
    Proc Natl Acad Sci U S A. 2007 Jun 26;104(26):11050-5 PMID: 17581883
  32. Structured surveillance of infantile gastroenteritis in East Anglia, UK: incidence of infection with common viral gastroenteric pathogens.
    Epidemiol Infect. 2008 Jan;136(1):23-33 PMID: 17313697
  33. Genetic polymorphism across regions of the three open reading frames of "Norwalk-like viruses".
    Arch Virol. 2000;145(2):223-41 PMID: 10752550
  34. Organization and expression of calicivirus genes.
    J Infect Dis. 2000 May;181 Suppl 2:S309-16 PMID: 10804143
  35. Taxonomy of the caliciviruses.
    J Infect Dis. 2000 May;181 Suppl 2:S322-30 PMID: 10804145
  36. Genetic classification of "Norwalk-like viruses..
    J Infect Dis. 2000 May;181 Suppl 2:S336-48 PMID: 10804147
  37. Possible emergence of new geminiviruses by frequent recombination.
    Virology. 1999 Dec 20;265(2):218-25 PMID: 10600594
  38. Characterization of a novel human calicivirus that may be a naturally occurring recombinant.
    Arch Virol. 1999;144(12):2377-87 PMID: 10664391
  39. Identification of an epitope common to genogroup 1 "norwalk-like viruses".
    J Clin Microbiol. 2000 Apr;38(4):1656-60 PMID: 10747162
  40. Norwalk virus open reading frame 3 encodes a minor structural protein.
    J Virol. 2000 Jul;74(14):6581-91 PMID: 10864672
  41. Interaction of cellular proteins with the 5' end of Norwalk virus genomic RNA.
    J Virol. 2000 Sep;74(18):8558-62 PMID: 10954557
  42. RDP: detection of recombination amongst aligned sequences.
    Bioinformatics. 2000 Jun;16(6):562-3 PMID: 10980155
  43. Sister-scanning: a Monte Carlo procedure for assessing signals in recombinant sequences.
    Bioinformatics. 2000 Jul;16(7):573-82 PMID: 11038328
  44. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach.
    Mol Biol Evol. 2001 May;18(5):691-9 PMID: 11319253
  45. MRBAYES: Bayesian inference of phylogenetic trees.
    Bioinformatics. 2001 Aug;17(8):754-5 PMID: 11524383
  46. The genome of hawaii virus and its relationship with other members of the caliciviridae.
    Virus Genes. 2001;23(1):5-16 PMID: 11556401
  47. Genetic classification of "Sapporo-like viruses".
    Arch Virol. 2001;146(11):2115-32 PMID: 11765915
  48. Structural requirements for the assembly of Norwalk virus-like particles.
    J Virol. 2002 Apr;76(8):4044-55 PMID: 11907243
  49. Natural history of human calicivirus infection: a prospective cohort study.
    Clin Infect Dis. 2002 Aug 1;35(3):246-53 PMID: 12115089
  50. Phylogenetic analysis of the complete genome of 18 Norwalk-like viruses.
    Virology. 2002 Aug 1;299(2):225-239 PMID: 12202225
  51. Molecular epidemiology of human calicivirus gastroenteritis outbreaks in Hungary, 1998 to 2000.
    J Med Virol. 2002 Nov;68(3):390-8 PMID: 12226827
  52. STAT1-dependent innate immunity to a Norwalk-like virus.
    Science. 2003 Mar 7;299(5612):1575-8 PMID: 12624267
  53. Broadly reactive and highly sensitive assay for Norwalk-like viruses based on real-time quantitative reverse transcription-PCR.
    J Clin Microbiol. 2003 Apr;41(4):1548-57 PMID: 12682144
  54. Processing of Norwalk virus nonstructural proteins by a 3C-like cysteine proteinase.
    Virology. 2003 Apr 10;308(2):216-24 PMID: 12706072
  55. Mfold web server for nucleic acid folding and hybridization prediction.
    Nucleic Acids Res. 2003 Jul 1;31(13):3406-15 PMID: 12824337
  56. Multiple sequence alignment with the Clustal series of programs.
    Nucleic Acids Res. 2003 Jul 1;31(13):3497-500 PMID: 12824352
  57. The 3' end of Norwalk virus mRNA contains determinants that regulate the expression and stability of the viral capsid protein VP1: a novel function for the VP2 protein.
    J Virol. 2003 Nov;77(21):11603-15 PMID: 14557646
  58. Mutations within the P2 domain of norovirus capsid affect binding to human histo-blood group antigens: evidence for a binding pocket.
    J Virol. 2003 Dec;77(23):12562-71 PMID: 14610179
  59. La, PTB, and PAB proteins bind to the 3(') untranslated region of Norwalk virus genomic RNA.
    Biochem Biophys Res Commun. 2003 Nov 21;311(3):759-66 PMID: 14623338
  60. Evolution of human calicivirus RNA in vivo: accumulation of mutations in the protruding P2 domain of the capsid leads to structural changes and possibly a new phenotype.
    J Virol. 2003 Dec;77(24):13117-24 PMID: 14645568
  61. Genetic diversity of norovirus and sapovirus in hospitalized infants with sporadic cases of acute gastroenteritis in Chiang Mai, Thailand.
    J Clin Microbiol. 2004 Mar;42(3):1305-7 PMID: 15004104
  62. Methods for the detection and characterisation of noroviruses associated with outbreaks of gastroenteritis: outbreaks occurring in the north-west of England during two norovirus seasons.
    J Med Virol. 2004 Jun;73(2):280-8 PMID: 15122805
  63. Chronic excretion of a norovirus in a child with cartilage hair hypoplasia (CHH).
    J Clin Virol. 2004 Jun;30(2):196-204 PMID: 15125877
  64. Outbreaks of acute gastroenteritis on cruise ships and on land: identification of a predominant circulating strain of norovirus--United States, 2002.
    J Infect Dis. 2004 Jul 1;190(1):27-36 PMID: 15195240
  65. Polyprotein processing in Southampton virus: identification of 3C-like protease cleavage sites by in vitro mutagenesis.
    J Virol. 1996 Apr;70(4):2605-10 PMID: 8642693
  66. Targeted disruption of the Stat1 gene in mice reveals unexpected physiologic specificity in the JAK-STAT signaling pathway.
    Cell. 1996 Feb 9;84(3):431-42 PMID: 8608597
  67. Molecular epidemiology of "Norwalk-like viruses" in outbreaks of gastroenteritis in the United States.
    J Infect Dis. 1998 Dec;178(6):1571-8 PMID: 9815206
  68. MODELTEST: testing the model of DNA substitution.
    Bioinformatics. 1998;14(9):817-8 PMID: 9918953
  69. Identification of further proteolytic cleavage sites in the Southampton calicivirus polyprotein by expression of the viral protease in E. coli.
    J Gen Virol. 1999 Feb;80 ( Pt 2):291-6 PMID: 10073687
  70. Identification of a distinct common strain of "Norwalk-like viruses" having a global distribution.
    J Infect Dis. 1999 Jun;179(6):1334-44 PMID: 10228052
  71. Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure.
    J Mol Biol. 1999 May 21;288(5):911-40 PMID: 10329189
  72. Food-related illness and death in the United States.
    Emerg Infect Dis. 1999 Sep-Oct;5(5):607-25 PMID: 10511517
  73. X-ray crystallographic structure of the Norwalk virus capsid.
    Science. 1999 Oct 8;286(5438):287-90 PMID: 10514371
  74. Replication of Norovirus in cell culture reveals a tropism for dendritic cells and macrophages.
    PLoS Biol. 2004 Dec;2(12):e432 PMID: 15562321
  75. RDP2: recombination detection and analysis from sequence alignments.
    Bioinformatics. 2005 Jan 15;21(2):260-2 PMID: 15377507
  76. Characteristics of human calicivirus enteritis in intestinal transplant recipients.
    J Pediatr Gastroenterol Nutr. 2005 Mar;40(3):328-33 PMID: 15735487
  77. Expression and antigenicity of virus-like particles of norovirus and their application for detection of noroviruses in stool samples.
    J Med Virol. 2005 May;76(1):129-36 PMID: 15778983
  78. Evidence of recombination in the norovirus capsid gene.
    J Virol. 2005 Apr;79(8):4977-90 PMID: 15795283
  79. Epitopes in the P2 domain of norovirus VP1 recognized by monoclonal antibodies that block cell interactions.
    J Gen Virol. 2005 Oct;86(Pt 10):2799-806 PMID: 16186235
  80. Characterization of new recombinant noroviruses.
    J Clin Microbiol. 2005 Oct;43(10):5179-86 PMID: 16207981
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
2007-10-00
Epub
2007-00-25
Pages
10460-73
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC2045448
Subset
IM
Grants
NIAID NIH HHS · R01 AI065982 · United States
NIAID NIH HHS · R01 AI54483 · United States
NIAID NIH HHS · T32-AI007163 · United States
NIAID NIH HHS · R01 AI054483 · United States
NCI NIH HHS · T32 CA009547 · United States
NIAID NIH HHS · T32 AI007163 · United States
NIAID NIH HHS · AI065982 · United States
NCI NIH HHS · T32-CA09547 · United States
NIAID NIH HHS · U54-AI057160 · United States
NIAID NIH HHS · U54 AI057160 · United States
Databases
GENBANK
EU004654, EU004655, EU004656, EU004657, EU004658, EU004659, EU004660, EU004661, EU004662, EU004663, EU004664, EU004665, EU004666, EU004667, EU004668, EU004669, EU004670, EU004671, EU004672, EU004673, EU004674, EU004675, EU004676, EU004677, EU004678, EU004679, EU004680, EU004681, EU004682, EU004683
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]