Home LiteratureArticle Details
PMID: 19074283 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

A critical link between Toll-like receptor 3 and type II interferon signaling pathways in antiviral innate immunity.

Negishi H, Osawa T, Ogami K, Ouyang X, Sakaguchi S, Koshiba R, Yanai H, Seko Y, Shitara H, Bishop K, Yonekawa H, Tamura T, Kaisho T, Taya C, Taniguchi T, Honda K

Abstract

A conundrum of innate antiviral immunity is how nucleic acid-sensing Toll-like receptors (TLRs) and RIG-I/MDA5 receptors cooperate during virus infection. The conventional wisdom has been that the activation of these receptor pathways evokes type I IFN (IFN) responses. Here, we provide evidence for a critical role of a Toll-like receptor 3 (TLR3)-dependent type II IFN signaling pathway in antiviral innate immune response against Coxsackievirus group B serotype 3 (CVB3), a member of the positive-stranded RNA virus family picornaviridae and most prevalent virus associated with chronic dilated cardiomyopathy. TLR3-deficient mice show a vulnerability to CVB3, accompanied by acute myocarditis, whereas transgenic expression of TLR3 endows even type I IFN signal-deficient mice resistance to CVB3 and other types of viruses, provided that type II IFN signaling remains intact. Taken together, our results indicate a critical cooperation of the RIG-I/MDA5-type I IFN and the TLR3-type II IFN signaling axes for efficient innate antiviral immune responses.

MeSH Terms
Animals DEAD Box Protein 58 DEAD-box RNA Helicases/metabolism Enterovirus/immunology Immunity, Innate Interferon Type I/immunology,metabolism Interferon-Induced Helicase, IFIH1 Interferon-gamma/immunology,metabolism Mice Mice, Knockout Myocarditis/immunology,virology Signal Transduction/immunology Toll-Like Receptor 3/deficiency,immunology,metabolism Virus Diseases/immunology
Chemicals
Interferon Type I TLR3 protein, mouse Toll-Like Receptor 3 Interferon-gamma Ddx58 protein, mouse Ifih1 protein, mouse DEAD Box Protein 58 DEAD-box RNA Helicases Interferon-Induced Helicase, IFIH1
Authors & Affiliations
16 authors, click to expand affiliations / ORCID
Negishi Hideo
Department of Immunology, Graduate School of Medicine and Faculty of Medicine, University of Tokyo, Hongo 7-3-1, Bunkyo-ku, Tokyo 113-0033, Japan.
Osawa Tomoko
Ogami Kentaro
Ouyang Xinshou
Sakaguchi Shinya
Koshiba Ryuji
Yanai Hideyuki
Seko Yoshinori
Shitara Hiroshi
Bishop Keith
Yonekawa Hiromichi
Tamura Tomohiko
Kaisho Tsuneyasu
Taya Choji
Taniguchi Tadatsugu
Honda Kenya
References (36)
36 references, click to expand
  1. Coxsackie B viruses and human heart disease.
    Curr Top Microbiol Immunol. 1997;223:31-52 PMID: 9294924
  2. Toll-like receptor 3 mediates West Nile virus entry into the brain causing lethal encephalitis.
    Nat Med. 2004 Dec;10(12):1366-73 PMID: 15558055
  3. Toll-like receptors 9 and 3 as essential components of innate immune defense against mouse cytomegalovirus infection.
    Proc Natl Acad Sci U S A. 2004 Mar 9;101(10):3516-21 PMID: 14993594
  4. Pancreatic expression of interferon-gamma protects mice from lethal coxsackievirus B3 infection and subsequent myocarditis.
    Nat Med. 2000 Jun;6(6):693-7 PMID: 10835688
  5. Protection from lethal coxsackievirus-induced pancreatitis by expression of gamma interferon.
    J Virol. 1999 Mar;73(3):1756-66 PMID: 9971752
  6. IFNs activate toll-like receptor gene expression in viral infections.
    Genes Immun. 2001 Oct;2(6):349-55 PMID: 11607792
  7. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3.
    Nature. 2001 Oct 18;413(6857):732-8 PMID: 11607032
  8. Cardioselective infection with coxsackievirus B3 requires intact type I interferon signaling: implications for mortality and early viral replication.
    Circulation. 2001 Feb 6;103(5):756-61 PMID: 11156890
  9. The interferon response circuit: induction and suppression by pathogenic viruses.
    Virology. 2006 Jan 5;344(1):119-30 PMID: 16364743
  10. RIG-I family RNA helicases: cytoplasmic sensor for antiviral innate immunity.
    Cytokine Growth Factor Rev. 2007 Oct-Dec;18(5-6):545-51 PMID: 17683970
  11. Selective contribution of IFN-alpha/beta signaling to the maturation of dendritic cells induced by double-stranded RNA or viral infection.
    Proc Natl Acad Sci U S A. 2003 Sep 16;100(19):10872-7 PMID: 12960379
  12. IFN-gamma production by antigen-presenting cells: mechanisms emerge.
    Trends Immunol. 2001 Oct;22(10):556-60 PMID: 11574279
  13. Immune defence in mice lacking type I and/or type II interferon receptors.
    Immunol Rev. 1995 Dec;148:5-18 PMID: 8825279
  14. Type I interferons in host defense.
    Immunity. 2006 Sep;25(3):373-81 PMID: 16979569
  15. Toll-like receptor 3 is an essential component of the innate stress response in virus-induced cardiac injury.
    Am J Physiol Heart Circ Physiol. 2007 Jan;292(1):H251-8 PMID: 16936008
  16. IRFs: master regulators of signalling by Toll-like receptors and cytosolic pattern-recognition receptors.
    Nat Rev Immunol. 2006 Sep;6(9):644-58 PMID: 16932750
  17. A missense mutation of the Toll-like receptor 3 gene in a patient with influenza-associated encephalopathy.
    Clin Immunol. 2006 May;119(2):188-94 PMID: 16517210
  18. Subcellular localization of Toll-like receptor 3 in human dendritic cells.
    J Immunol. 2003 Sep 15;171(6):3154-62 PMID: 12960343
  19. CVB infection and mechanisms of viral cardiomyopathy.
    Curr Top Microbiol Immunol. 2008;323:315-35 PMID: 18357777
  20. Sensing of viral infection and activation of innate immunity by toll-like receptor 3.
    Clin Microbiol Rev. 2008 Jan;21(1):13-25 PMID: 18202435
  21. Intracellular pattern recognition receptors in the host response.
    Nature. 2006 Jul 6;442(7098):39-44 PMID: 16823444
  22. Effects of in vivo administration of anti-B7-1/B7-2 monoclonal antibodies on murine acute myocarditis caused by coxsackievirus B3.
    Circ Res. 1998 Mar 23;82(5):613-8 PMID: 9529166
  23. Viruses and interferon: a fight for supremacy.
    Nat Rev Immunol. 2002 Sep;2(9):675-87 PMID: 12209136
  24. Detrimental contribution of the Toll-like receptor (TLR)3 to influenza A virus-induced acute pneumonia.
    PLoS Pathog. 2006 Jun;2(6):e53 PMID: 16789835
  25. Essential role of mda-5 in type I IFN responses to polyriboinosinic:polyribocytidylic acid and encephalomyocarditis picornavirus.
    Proc Natl Acad Sci U S A. 2006 May 30;103(22):8459-64 PMID: 16714379
  26. Plasmacytoid dendritic cells: sensing nucleic acids in viral infection and autoimmune diseases.
    Nat Rev Immunol. 2008 Aug;8(8):594-606 PMID: 18641647
  27. Interferon-gamma: an overview of signals, mechanisms and functions.
    J Leukoc Biol. 2004 Feb;75(2):163-89 PMID: 14525967
  28. Host immune responses to coxsackievirus B3.
    Curr Top Microbiol Immunol. 2008;323:199-221 PMID: 18357771
  29. Structural mechanism of RNA recognition by the RIG-I-like receptors.
    Immunity. 2008 Aug 15;29(2):178-81 PMID: 18701081
  30. Toll-like receptor 3 has a protective role against West Nile virus infection.
    J Virol. 2008 Nov;82(21):10349-58 PMID: 18715906
  31. Immune response in mice that lack the interferon-gamma receptor.
    Science. 1993 Mar 19;259(5102):1742-5 PMID: 8456301
  32. Recognition of microorganisms and activation of the immune response.
    Nature. 2007 Oct 18;449(7164):819-26 PMID: 17943118
  33. Parallels among positive-strand RNA viruses, reverse-transcribing viruses and double-stranded RNA viruses.
    Nat Rev Microbiol. 2006 May;4(5):371-82 PMID: 16582931
  34. IRF-7 is the master regulator of type-I interferon-dependent immune responses.
    Nature. 2005 Apr 7;434(7034):772-7 PMID: 15800576
  35. Does Toll-like receptor 3 play a biological role in virus infections?
    Virology. 2004 May 1;322(2):231-8 PMID: 15110521
  36. TLR3 deficiency in patients with herpes simplex encephalitis.
    Science. 2007 Sep 14;317(5844):1522-7 PMID: 17872438
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2008-12-23
Epub
2008-00-11
Pages
20446-51
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC2629334
Subset
IM
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