Home LiteratureArticle Details
PMID: 22258242 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Protruding domain of capsid protein is necessary and sufficient to determine murine norovirus replication and pathogenesis in vivo.

Journal of virology ·Vol. 86 ·No. 6 ·2012-03-00 ·Pages 2950-8

Strong DW, Thackray LB, Smith TJ, Virgin HW

Abstract

Human noroviruses (HuNoVs) are the major cause of epidemic, nonbacterial gastroenteritis worldwide. Due to the lack of a tractable model system and the inability to grow HuNoVs in cell culture, factors required for the norovirus (NoV) life cycle and pathogenesis in the host remain largely unknown. The discovery of murine norovirus (MNV) and the development of reverse-genetics systems for this virus provide an opportunity to study these aspects of NoV infection in vitro and in vivo. Previous studies identified a single amino acid at residue 296 in the protruding (P) domain of the capsid protein that is responsible for determining the virulence of the MNV clone MNV1.CW1 in 12956/SvEv background STAT1-deficient (STAT1(-/-)) mice. In this report, we identified and characterized another determinant of lethality in the P domain that is necessary and sufficient to determine the replication and pathogenesis of the MNV clones MNV1.CW3 and CR6.STL1 in C57BL/6 background STAT1(-/-) mice. Furthermore, we describe how the role of residue 296 in MNV virulence differs between STAT1(-/-) mouse strains. We also describe potential interactions between subdomains of the P domain, as well as between other virus elements, which facilitate recovery of MNV using a reverse-genetics system.

MeSH Terms
Animals Caliciviridae Infections/virology Capsid Proteins/chemistry,genetics,metabolism Cell Line Mice Mice, Inbred C57BL Mice, Knockout Molecular Sequence Data Norovirus/chemistry,genetics,pathogenicity,physiology Protein Structure, Tertiary Virulence Virus Replication
Chemicals
Capsid Proteins
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Strong David W
Department of Pathology and Immunology, Washington University School of Medicine, St. Louis, Missouri, USA.
Thackray Larissa B
Smith Tom J
Virgin Herbert W
References (65)
65 references, click to expand
  1. Prevalence and characteristics of asymptomatic norovirus infection in the community in England.
    Epidemiol Infect. 2010 Oct;138(10):1454-8 PMID: 20196905
  2. Replication of Norovirus in cell culture reveals a tropism for dendritic cells and macrophages.
    PLoS Biol. 2004 Dec;2(12):e432 PMID: 15562321
  3. Murine noroviruses comprising a single genogroup exhibit biological diversity despite limited sequence divergence.
    J Virol. 2007 Oct;81(19):10460-73 PMID: 17652401
  4. Diversity of murine norovirus strains isolated from asymptomatic mice of different genetic backgrounds within a single U.S. research institute.
    PLoS One. 2011;6(6):e21435 PMID: 21738664
  5. Norovirus capture with histo-blood group antigens reveals novel virus-ligand interactions.
    J Virol. 2004 Mar;78(6):3035-45 PMID: 14990722
  6. Calicivirus translation initiation requires an interaction between VPg and eIF 4 E.
    EMBO Rep. 2005 Oct;6(10):968-72 PMID: 16142217
  7. Chronic norovirus infection in renal transplant recipients.
    Nephrol Dial Transplant. 2009 Mar;24(3):1051-3 PMID: 19073655
  8. The natural host range shift and subsequent evolution of canine parvovirus resulted from virus-specific binding to the canine transferrin receptor.
    J Virol. 2003 Feb;77(3):1718-26 PMID: 12525605
  9. Recovery of genetically defined murine norovirus in tissue culture by using a fowlpox virus expressing T7 RNA polymerase.
    J Gen Virol. 2007 Aug;88(Pt 8):2091-2100 PMID: 17622609
  10. Norwalk virus infection and disease is associated with ABO histo-blood group type.
    J Infect Dis. 2002 May 1;185(9):1335-7 PMID: 12001052
  11. Assessing the genetic component of the susceptibility of mice to viral infections.
    Brief Funct Genomic Proteomic. 2005 Nov;4(3):225-40 PMID: 16420748
  12. Norwalk virus shedding after experimental human infection.
    Emerg Infect Dis. 2008 Oct;14(10):1553-7 PMID: 18826818
  13. The epidemiologic and clinical importance of norovirus infection.
    Gastroenterol Clin North Am. 2006 Jun;35(2):275-90, viii PMID: 16880066
  14. Noroviruses: a comprehensive review.
    J Clin Virol. 2009 Jan;44(1):1-8 PMID: 19084472
  15. High-resolution x-ray structure and functional analysis of the murine norovirus 1 capsid protein protruding domain.
    J Virol. 2010 Jun;84(11):5695-705 PMID: 20335262
  16. An outbreak of necrotizing enterocolitis associated with norovirus genotype GII.3.
    Pediatr Infect Dis J. 2010 Jul;29(7):644-7 PMID: 20589982
  17. Different mechanisms of antibody-mediated neutralization of parvoviruses revealed using the Fab fragments of monoclonal antibodies.
    Virology. 2007 May 10;361(2):283-93 PMID: 17217977
  18. Human noroviruses recognize sialyl Lewis x neoglycoprotein.
    Glycobiology. 2009 Mar;19(3):309-20 PMID: 19054801
  19. Evolution to pathogenicity of the parvovirus minute virus of mice in immunodeficient mice involves genetic heterogeneity at the capsid domain that determines tropism.
    J Virol. 2008 Feb;82(3):1195-203 PMID: 18045943
  20. Molecular characterization of three novel murine noroviruses.
    Virus Genes. 2007 Apr;34(2):147-55 PMID: 17171545
  21. Ganglioside-linked terminal sialic acid moieties on murine macrophages function as attachment receptors for murine noroviruses.
    J Virol. 2009 May;83(9):4092-101 PMID: 19244326
  22. Comparative murine norovirus studies reveal a lack of correlation between intestinal virus titers and enteric pathology.
    Virology. 2011 Dec 20;421(2):202-10 PMID: 22018636
  23. Targeted disruption of the mouse Stat1 gene results in compromised innate immunity to viral disease.
    Cell. 1996 Feb 9;84(3):443-50 PMID: 8608598
  24. VPg of murine norovirus binds translation initiation factors in infected cells.
    Virol J. 2006 May 23;3:33 PMID: 16719923
  25. 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
  26. Norovirus gastroenteritis causes severe and lethal complications after chemotherapy and hematopoietic stem cell transplantation.
    Blood. 2011 Jun 2;117(22):5850-6 PMID: 21487110
  27. Bioinformatic and functional analysis of RNA secondary structure elements among different genera of human and animal caliciviruses.
    Nucleic Acids Res. 2008 May;36(8):2530-46 PMID: 18319285
  28. Type I and type II interferons inhibit the translation of murine norovirus proteins.
    J Virol. 2009 Jun;83(11):5683-92 PMID: 19297466
  29. Cleavage map and proteolytic processing of the murine norovirus nonstructural polyprotein in infected cells.
    J Virol. 2006 Aug;80(16):7816-31 PMID: 16873239
  30. Norwalk virus open reading frame 3 encodes a minor structural protein.
    J Virol. 2000 Jul;74(14):6581-91 PMID: 10864672
  31. Norwalk virus infection of volunteers: new insights based on improved assays.
    J Infect Dis. 1994 Jul;170(1):34-43 PMID: 8014518
  32. High-resolution cryo-electron microscopy structures of murine norovirus 1 and rabbit hemorrhagic disease virus reveal marked flexibility in the receptor binding domains.
    J Virol. 2010 Jun;84(11):5836-41 PMID: 20335264
  33. STAT1-dependent innate immunity to a Norwalk-like virus.
    Science. 2003 Mar 7;299(5612):1575-8 PMID: 12624267
  34. Virulent variants emerging in mice infected with the apathogenic prototype strain of the parvovirus minute virus of mice exhibit a capsid with low avidity for a primary receptor.
    J Virol. 2005 Sep;79(17):11280-90 PMID: 16103180
  35. Norovirus encephalopathy in a previously healthy child.
    Pediatr Infect Dis J. 2010 Nov;29(11):1057-9 PMID: 20555291
  36. Antibody is critical for the clearance of murine norovirus infection.
    J Virol. 2008 Jul;82(13):6610-7 PMID: 18417579
  37. Viral shape-shifting: norovirus evasion of the human immune system.
    Nat Rev Microbiol. 2010 Mar;8(3):231-41 PMID: 20125087
  38. Structures of host range-controlling regions of the capsids of canine and feline parvoviruses and mutants.
    J Virol. 2003 Nov;77(22):12211-21 PMID: 14581558
  39. Immune mechanisms responsible for vaccination against and clearance of mucosal and lymphatic norovirus infection.
    PLoS Pathog. 2008 Dec;4(12):e1000236 PMID: 19079577
  40. Norovirus classification and proposed strain nomenclature.
    Virology. 2006 Mar 15;346(2):312-23 PMID: 16343580
  41. Norovirus infection as a cause of diarrhea-associated benign infantile seizures.
    Clin Infect Dis. 2009 Apr 1;48(7):849-55 PMID: 19239351
  42. Noroviruses bind to human ABO, Lewis, and secretor histo-blood group antigens: identification of 4 distinct strain-specific patterns.
    J Infect Dis. 2003 Jul 1;188(1):19-31 PMID: 12825167
  43. Murine gammaherpesvirus 68 infection is associated with lymphoproliferative disease and lymphoma in BALB beta2 microglobulin-deficient mice.
    J Virol. 2005 Dec;79(23):14668-79 PMID: 16282467
  44. MDA-5 recognition of a murine norovirus.
    PLoS Pathog. 2008 Jul 18;4(7):e1000108 PMID: 18636103
  45. Norovirus regulation of the innate immune response and apoptosis occurs via the product of the alternative open reading frame 4.
    PLoS Pathog. 2011 Dec;7(12):e1002413 PMID: 22174679
  46. 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
  47. Norovirus RNA in the blood of a child with gastroenteritis and convulsions--A case report.
    J Clin Virol. 2010 Jun;48(2):147-9 PMID: 20381416
  48. Structural determinants of tissue tropism and in vivo pathogenicity for the parvovirus minute virus of mice.
    J Virol. 2005 Sep;79(17):10931-43 PMID: 16103145
  49. Virus-plus-susceptibility gene interaction determines Crohn's disease gene Atg16L1 phenotypes in intestine.
    Cell. 2010 Jun 25;141(7):1135-45 PMID: 20602997
  50. Excess mortality following community-onset norovirus enteritis in the elderly.
    J Hosp Infect. 2011 Sep;79(1):27-31 PMID: 21764172
  51. Diversity of murine norovirus in wild-rodent populations: species-specific associations suggest an ancient divergence.
    J Gen Virol. 2012 Feb;93(Pt 2):259-266 PMID: 22071511
  52. Murine norovirus, a recently discovered and highly prevalent viral agent of mice.
    Lab Anim (NY). 2008 Jul;37(7):314-20 PMID: 18568010
  53. Functional analysis of RNA structures present at the 3' extremity of the murine norovirus genome: the variable polypyrimidine tract plays a role in viral virulence.
    J Virol. 2010 Mar;84(6):2859-70 PMID: 20053745
  54. Postinfectious irritable bowel syndrome after a food-borne outbreak of acute gastroenteritis attributed to a viral pathogen.
    Clin Gastroenterol Hepatol. 2007 Apr;5(4):457-60 PMID: 17289440
  55. Outbreak of necrotizing enterocolitis caused by norovirus in a neonatal intensive care unit.
    J Pediatr. 2008 Sep;153(3):339-44 PMID: 18534621
  56. Structure of antibody-neutralized murine norovirus and unexpected differences from viruslike particles.
    J Virol. 2008 Mar;82(5):2079-88 PMID: 18094184
  57. Persistent infection with and serologic cross-reactivity of three novel murine noroviruses.
    Comp Med. 2006 Aug;56(4):247-51 PMID: 16941951
  58. 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
  59. Norovirus gastroenteritis.
    N Engl J Med. 2009 Oct 29;361(18):1776-85 PMID: 19864676
  60. Unspecified gastroenteritis illness and deaths in the elderly associated with norovirus epidemics.
    Epidemiology. 2011 May;22(3):336-43 PMID: 21358409
  61. Mechanisms of GII.4 norovirus persistence in human populations.
    PLoS Med. 2008 Feb;5(2):e31 PMID: 18271619
  62. A single amino acid substitution in the murine norovirus capsid protein is sufficient for attenuation in vivo.
    J Virol. 2008 Aug;82(15):7725-8 PMID: 18495770
  63. 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
  64. Murine norovirus: a model system to study norovirus biology and pathogenesis.
    J Virol. 2006 Jun;80(11):5104-12 PMID: 16698991
  65. Structural requirements for the assembly of Norwalk virus-like particles.
    J Virol. 2002 Apr;76(8):4044-55 PMID: 11907243
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
1098-5514
Published
2012-03-00
Epub
2012-00-18
Pages
2950-8
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC3302348
Subset
IM
Grants
NIAID NIH HHS · R01 AI054483 · United States
PHS HHS · 5T32A100716334 · United States
NIAID NIH HHS · AI0544483 · United States
Databases
GENBANK
JQ237823
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: product@genelibs.com