Home LiteratureArticle Details
PMID: 17229692 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Murine norovirus 1 infection is associated with histopathological changes in immunocompetent hosts, but clinical disease is prevented by STAT1-dependent interferon responses.

Journal of virology ·Vol. 81 ·No. 7 ·2007-04-00 ·Pages 3251-63

Mumphrey SM, Changotra H, Moore TN, Heimann-Nichols ER, Wobus CE, Reilly MJ, Moghadamfalahi M, Shukla D, Karst SM

Abstract

Human noroviruses are the major cause of nonbacterial epidemic gastroenteritis worldwide. However, little is known regarding their pathogenesis or the immune responses that control them because until recently there has been no small animal model or cell culture system of norovirus infection. We recently reported the discovery of the first murine norovirus, murine norovirus 1 (MNV-1), and its cultivation in macrophages and dendritic cells in vitro. We further defined interferon receptors and the STAT-1 molecule as critical in both resistance to MNV-1-induced disease in vivo and control of virus growth in vitro. To date, neither histopathological changes upon infection nor viral replication in wild-type mice has been shown. Here we extend our studies to demonstrate that MNV-1 replicates and rapidly disseminates to various tissues in immunocompetent mice and that infection is restricted by STAT1-dependent interferon responses at the levels of viral replication and virus dissemination. Infection of wild-type mice is associated with histopathological alterations in the intestine (mild inflammation) and the spleen (red pulp hypertrophy and white pulp activation); viral dissemination to the spleen, liver, lung, and lymph nodes; and low-level persistent infection in the spleen. STAT-1 inhibits viral replication in the intestine, prevents virus-induced apoptosis of intestinal cells and splenocytes, and limits viral dissemination to peripheral tissues. These findings demonstrate that murine norovirus infection of wild-type mice is associated with initial enteric seeding and subsequent extraintestinal spread, and they provide mechanistic evidence of the role of STAT-1 in controlling clinical norovirus-induced disease.

MeSH Terms
Animals Biomarkers Caliciviridae Infections/immunology,metabolism,pathology,virology Cell Line Gastroenteritis/genetics,metabolism,pathology,virology Interferons/metabolism Kinetics Mice Mice, Transgenic Norovirus/immunology,isolation & purification STAT1 Transcription Factor/deficiency,genetics,metabolism Spleen/immunology,metabolism,pathology,virology Time Factors Virus Replication
Chemicals
Biomarkers STAT1 Transcription Factor Stat1 protein, mouse Interferons
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Mumphrey Shannon M
Center for Molecular and Tumor Virology, Department of Microbiology and Immunology, Louisiana State University Health Sciences Center, 1501 Kings Highway, Shreveport, LA 71130, USA.
Changotra Harish
Moore Tara N
Heimann-Nichols Ellen R
Wobus Christiane E
Reilly Michael J
Moghadamfalahi Mana
Shukla Deepti
Karst Stephanie M
References (47)
47 references, click to expand
  1. Abnormal gastric motor function in viral gastroenteritis.
    Ann Intern Med. 1980 Mar;92(3):370-3 PMID: 6766695
  2. Immune response and prevalence of antibody to Norwalk enteritis virus as determined by radioimmunoassay.
    J Clin Microbiol. 1979 Dec;10(6):903-9 PMID: 118178
  3. Multiple-challenge study of host susceptibility to Norwalk gastroenteritis in US adults.
    J Infect Dis. 1990 Jan;161(1):18-21 PMID: 2153184
  4. An enzyme-linked immunosorbent assay for detection of antibodies to maedi-visna virus in sheep. I. A simple technique for production of antigen using sodium dodecyl sulfate treatment.
    Can J Vet Res. 1990 Oct;54(4):446-50 PMID: 2174295
  5. Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins.
    Science. 1994 Jun 3;264(5164):1415-21 PMID: 8197455
  6. Norwalk virus infection of volunteers: new insights based on improved assays.
    J Infect Dis. 1994 Jul;170(1):34-43 PMID: 8014518
  7. 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
  8. Murine model of rotavirus infection.
    Adv Exp Med Biol. 1997;412:233-40 PMID: 9192019
  9. 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
  10. Replication of Norovirus in cell culture reveals a tropism for dendritic cells and macrophages.
    PLoS Biol. 2004 Dec;2(12):e432 PMID: 15562321
  11. Viraemia is a common finding in immunocompetent children with rotavirus infection.
    J Med Virol. 2005 Jun;76(2):265-7 PMID: 15834882
  12. Critical roles for both STAT1-dependent and STAT1-independent pathways in the control of primary dengue virus infection in mice.
    J Immunol. 2005 Sep 15;175(6):3946-54 PMID: 16148142
  13. 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
  14. Rotavirus viremia and extraintestinal viral infection in the neonatal rat model.
    J Virol. 2006 May;80(10):4820-32 PMID: 16641274
  15. Murine norovirus: a model system to study norovirus biology and pathogenesis.
    J Virol. 2006 Jun;80(11):5104-12 PMID: 16698991
  16. Extraintestinal spread and replication of a homologous EC rotavirus strain and a heterologous rhesus rotavirus in BALB/c mice.
    J Virol. 2006 Jun;80(11):5219-32 PMID: 16699002
  17. Active viremia in rotavirus-infected mice.
    J Virol. 2006 Jul;80(13):6702-5 PMID: 16775359
  18. Norovirus-associated encephalopathy.
    Pediatr Infect Dis J. 2006 Jul;25(7):651-2 PMID: 16804441
  19. Cleavage map and proteolytic processing of the murine norovirus nonstructural polyprotein in infected cells.
    J Virol. 2006 Aug;80(16):7816-31 PMID: 16873239
  20. Noroviruses everywhere: has something changed?
    Curr Opin Infect Dis. 2006 Oct;19(5):467-74 PMID: 16940871
  21. Persistent infection with and serologic cross-reactivity of three novel murine noroviruses.
    Comp Med. 2006 Aug;56(4):247-51 PMID: 16941951
  22. Pathology of immunodeficient mice with naturally occurring murine norovirus infection.
    Toxicol Pathol. 2006;34(6):708-15 PMID: 17074739
  23. Norwalk-like virus infection in military forces: epidemic potential, sporadic disease, and the future direction of prevention and control efforts.
    J Infect Dis. 2000 May;181 Suppl 2:S387-91 PMID: 10804153
  24. Epizootic vesicular disease in captive California sea lions.
    J Wildl Dis. 2000 Jul;36(3):500-7 PMID: 10941736
  25. Distinct requirements for IFNs and STAT1 in NK cell function.
    J Immunol. 2000 Oct 1;165(7):3571-7 PMID: 11034357
  26. Stat1-independent regulation of gene expression in response to IFN-gamma.
    Proc Natl Acad Sci U S A. 2001 Jun 5;98(12):6674-9 PMID: 11390994
  27. Biologic consequences of Stat1-independent IFN signaling.
    Proc Natl Acad Sci U S A. 2001 Jun 5;98(12):6680-5 PMID: 11390995
  28. Stat1-dependent and -independent pathways in IFN-gamma-dependent signaling.
    Trends Immunol. 2002 Feb;23(2):96-101 PMID: 11929133
  29. Cytokine signaling in 2002: new surprises in the Jak/Stat pathway.
    Cell. 2002 Apr;109 Suppl:S121-31 PMID: 11983158
  30. Outbreak of acute gastroenteritis associated with Norwalk-like viruses among British military personnel--Afghanistan, May 2002.
    MMWR Morb Mortal Wkly Rep. 2002 Jun 7;51(22):477-9 PMID: 12064451
  31. Natural history of human calicivirus infection: a prospective cohort study.
    Clin Infect Dis. 2002 Aug 1;35(3):246-53 PMID: 12115089
  32. STAT1-dependent innate immunity to a Norwalk-like virus.
    Science. 2003 Mar 7;299(5612):1575-8 PMID: 12624267
  33. An epizootic of highly virulent feline calicivirus disease in a hospital setting in New England.
    J Feline Med Surg. 2003 Aug;5(4):217-26 PMID: 12878149
  34. Laboratory diagnosis of norovirus: which method is the best?
    Intervirology. 2003;46(4):232-8 PMID: 12931032
  35. Outbreak of rabbit hemorrhagic disease in domestic lagomorphs.
    J Am Vet Med Assoc. 2003 Oct 15;223(8):1151-5, 1128 PMID: 14584745
  36. Rotavirus antigenaemia and viraemia: a common event?
    Lancet. 2003 Nov 1;362(9394):1445-9 PMID: 14602437
  37. Laboratory efforts to cultivate noroviruses.
    J Gen Virol. 2004 Jan;85(Pt 1):79-87 PMID: 14718622
  38. Increase in viral gastroenteritis outbreaks in Europe and epidemic spread of new norovirus variant.
    Lancet. 2004 Feb 28;363(9410):682-8 PMID: 15001325
  39. Clinical manifestation of norovirus gastroenteritis in health care settings.
    Clin Infect Dis. 2004 Aug 1;39(3):318-24 PMID: 15306997
  40. Feline picornavirus infection: the in vivo carrier state.
    Vet Rec. 1973 Mar 3;92(9):224-9 PMID: 4705874
  41. The mucosal lesion of the proximal small intestine in acute infectious nonbacterial gastroenteritis.
    N Engl J Med. 1973 Jun 21;288(25):1318-23 PMID: 4706274
  42. Acute infectious nonbacterial gastroenteritis: intestinal histopathology. Histologic and enzymatic alterations during illness produced by the Norwalk agent in man.
    Ann Intern Med. 1973 Jul;79(1):18-25 PMID: 4721173
  43. The small intestinal lesion induced by Hawaii agent acute infectious nonbacterial gastroenteritis.
    J Infect Dis. 1974 Jun;129(6):705-8 PMID: 4209259
  44. Viral gastroenteritis induced by the Hawaii agent. Jejunal histopathology and serologic response.
    Am J Med. 1975 Dec;59(6):761-8 PMID: 811119
  45. Clinical immunity in acute gastroenteritis caused by Norwalk agent.
    N Engl J Med. 1977 Jul 14;297(2):86-9 PMID: 405590
  46. The clinical disease and patterns of excretion associated with three different strains of feline caliciviruses.
    Res Vet Sci. 1977 Jul;23(1):7-14 PMID: 905658
  47. The effects of host age, virus dose, and virus strain on heterologous rotavirus infection of suckling mice.
    Microb Pathog. 1988 Mar;4(3):189-202 PMID: 2848173
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
2007-04-00
Epub
2007-00-17
Pages
3251-63
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC1866040
Subset
IM
Grants
NIAID NIH HHS · U54 AI 057160 · United States
NIAID NIH HHS · R01 AI054483 · United States
NIAID NIH HHS · R01 AI 54483 · United States
NCRR NIH HHS · P20 RR018724 · United States
NCRR NIH HHS · P20 RR 018724 · United States
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