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J. Biol. Chem., Vol. 280, Issue 1, 277-283, January 7, 2005
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Double-stranded RNAs from the Helminth Parasite Schistosoma Activate TLR3 in Dendritic Cells*
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From the
INSERM U547, Institut Pasteur de Lille, Lille, 59019 France, Institute for Medical Immunology, Université Libre de Bruxelles, B-1070 Brussels, Belgium, **Department of Biotechnology and Bioscience, University of Milano-Bicocca, 20126 Milan, Italy, CNRS, 8147 and Université Paris V, Hôpital Necker, 75743 Paris, France, and Laboratoire de Génétique Expérimentale et Moléculaire (GEM2358), CNRS, 41500 Orléans, France
Stimulation of dendritic cells (DCs) by the egg stage of the helminth parasite Schistosoma mansoni activates a signaling pathway resulting in type I interferon (IFN) and IFN-stimulated gene (ISG) expression. Here, we demonstrate that S. mansoni eggs disjointedly activate myeloid differentiation factor 88 (MyD88)-dependent and MyD88-independent pathways in DCs. Inflammatory cytokine expression and NF-
B activation in DCs from MyD88-deficient mice were impaired, whereas signaling transducer activator of transcription (STAT) 1(Tyr701) phosphorylation and ISG expression were intact in MyD88 or Toll-like receptor (TLR)4-deficient counterparts. Accordingly, we analyzed distinct TLR members for their ability to respond to schistosome eggs and established that TLR3 resulted in the activation of NF-B and the positive regulatory domain III-I site from IFN-
promoter. Unexpectedly, egg-derived RNA possessed RNase A-resistant and RNase III-sensitive structures capable of triggering TLR3 activation, suggesting the involvement of double-stranded (ds) structures. Moreover, DCs from TLR3-deficient mice displayed a complete loss of signaling transducer activator of transcription 1 phosphorylation and ISG expression in response to egg-derived dsRNA. Finally, TLR3-deficient DCs showed a reduced response to schistosome eggs relative to wild-type cells. Collectively, our data suggest for the first time that dsRNA from a non-viral pathogen may act as an inducer of the innate immune system through TLR3.
Received for publication, September 30, 2004
* The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
The on-line version of this article (available at http://www.jbc.org) contains Supplemental Fig. S1.
¶ Supported by a Belgium Télevie grant.
|| Supported by a French Ministry of National Education, Research, and Technology grant.
¶¶ To whom correspondence should be addressed: Centre d'Immunologie et Biologie Parasitaire, INSERM U547, 1 rue du Professeur Calmette, Institut Pasteur de LILLE, 59019 Lille, France. Tel.: 33-3-20-877-885; Fax: 33-3-20-877-888; E-mail: francois.trottein{at}pasteurlille.fr.
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