Recognition of double-stranded RNA by human toll-like receptor 3 and downstream receptor signaling requires multimerization and an acidic pH.
Identifieur interne : 002313 ( PubMed/Corpus ); précédent : 002312; suivant : 002314Recognition of double-stranded RNA by human toll-like receptor 3 and downstream receptor signaling requires multimerization and an acidic pH.
Auteurs : Odette De Bouteiller ; Estelle Merck ; Uzma A. Hasan ; Sylvain Hubac ; Barbara Benguigui ; Giorgio Trinchieri ; Elizabeth E M. Bates ; Christophe CauxSource :
- The Journal of biological chemistry [ 0021-9258 ] ; 2005.
English descriptors
- KwdEn :
- Amino Acid Sequence, Antigens, CD (chemistry), Antirheumatic Agents (pharmacology), Base Sequence, Binding Sites, Blotting, Western, Calcium (metabolism), Cell Line, Cell Membrane (metabolism), Cell Separation, Chloroquine (chemistry), Cross-Linking Reagents (pharmacology), Cysteine (chemistry), Cysteine (metabolism), Cytokines (metabolism), DNA (metabolism), Dendritic Cells (metabolism), Dimerization, Dose-Response Relationship, Drug, Endosomes (metabolism), Enzyme Inhibitors (pharmacology), Flow Cytometry, Genes, Dominant, Genes, Reporter, Glycosylation, Humans, Hydrogen-Ion Concentration, Leucine (chemistry), Leukocytes, Mononuclear (metabolism), Ligands, Luciferases (metabolism), Lysosomes (chemistry), Lysosomes (metabolism), Macrolides (pharmacology), Molecular Sequence Data, Mutagenesis, Site-Directed, Mutation, NF-kappa B (metabolism), Phagosomes (chemistry), Protein Binding, Protein Structure, Tertiary, Receptors, IgG (biosynthesis), Receptors, IgG (chemistry), Recombinant Fusion Proteins (chemistry), Recombinant Fusion Proteins (metabolism), Sequence Homology, Amino Acid, Signal Transduction, Time Factors, Toll-Like Receptor 3 (chemistry), Toll-Like Receptor 3 (metabolism), Transfection, Tyrosine (chemistry), U937 Cells.
- MESH :
- chemical , biosynthesis : Receptors, IgG.
- chemical , chemistry : Antigens, CD, Chloroquine, Cysteine, Leucine, Receptors, IgG, Recombinant Fusion Proteins, Toll-Like Receptor 3, Tyrosine.
- chemical , metabolism : Calcium, Cysteine, Cytokines, DNA, Luciferases, NF-kappa B, Recombinant Fusion Proteins, Toll-Like Receptor 3.
- chemical , pharmacology : Antirheumatic Agents, Cross-Linking Reagents, Enzyme Inhibitors, Macrolides.
- chemistry : Lysosomes, Phagosomes.
- metabolism : Cell Membrane, Dendritic Cells, Endosomes, Leukocytes, Mononuclear, Lysosomes.
- Amino Acid Sequence, Base Sequence, Binding Sites, Blotting, Western, Cell Line, Cell Separation, Dimerization, Dose-Response Relationship, Drug, Flow Cytometry, Genes, Dominant, Genes, Reporter, Glycosylation, Humans, Hydrogen-Ion Concentration, Ligands, Molecular Sequence Data, Mutagenesis, Site-Directed, Mutation, Protein Binding, Protein Structure, Tertiary, Sequence Homology, Amino Acid, Signal Transduction, Time Factors, Transfection, U937 Cells.
Abstract
Studies involving Toll-like receptor 3 (TLR3)-deficient mice suggest that this receptor binds double-stranded RNA. In the present study, we analyzed ligand/receptor interactions and receptor-proximal events leading to TLR3 activation. The mutagenesis approach showed that certain cysteine residues and glycosylation in TLR3 amino-terminal leucine-rich repeats were necessary for ligand-induced signaling. Furthermore, inactive mutants had a dominant negative effect, suggesting that the signaling module is a multimer. We constructed a chimeric molecule fusing the amino-terminal ectodomain of TLR3 to the transmembrane and carboxyl terminal domains of CD32a containing an immunoreceptor tyrosine-based motif. Expression of TLR3-CD32 in HEK293T cells and the myeloid cell line U937 resulted in surface localization of the receptor, whereas the nonrecombinant molecule was intracellularly localized. The synthetic double-stranded RNAs poly(I-C) and poly(A-U) induced calcium mobilization in a TLR3-CD32 stably transfected U937 clone but not in control cells transfected with other constructs. An anti-TLR3 antibody also induced Ca(2+) flux but only when cross-linked by a secondary anti-immunoglobulin antibody, confirming that multimerization by the ligand is a requirement for signaling. The inhibitors of lysosome maturation, bafilomycin and chloroquine, inhibited the poly(I-C)-induced biological response in immune cells, showing that TLR3 interacted with its ligand in acidic subcellular compartments. Furthermore, TLR3-CD32 activation with poly(I-C) was only observed within a narrow pH window (pH 5.7-6.7), whereas anti-TLR3-mediated Ca(2+) flux was pH-insensitive. The importance of an acidic pH for TLR3-ligand interaction becomes critical when using oligomeric poly(I-C) (15-40-mers). These observations demonstrate that engagement of TLR3 by poly(I-C) at an acidic pH, probably in early phagolysosomes or endosomes, induces receptor aggregation leading to signaling.
DOI: 10.1074/jbc.M507163200
PubMed: 16144834
Links to Exploration step
pubmed:16144834Le document en format XML
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<term>Antirheumatic Agents (pharmacology)</term>
<term>Base Sequence</term>
<term>Binding Sites</term>
<term>Blotting, Western</term>
<term>Calcium (metabolism)</term>
<term>Cell Line</term>
<term>Cell Membrane (metabolism)</term>
<term>Cell Separation</term>
<term>Chloroquine (chemistry)</term>
<term>Cross-Linking Reagents (pharmacology)</term>
<term>Cysteine (chemistry)</term>
<term>Cysteine (metabolism)</term>
<term>Cytokines (metabolism)</term>
<term>DNA (metabolism)</term>
<term>Dendritic Cells (metabolism)</term>
<term>Dimerization</term>
<term>Dose-Response Relationship, Drug</term>
<term>Endosomes (metabolism)</term>
<term>Enzyme Inhibitors (pharmacology)</term>
<term>Flow Cytometry</term>
<term>Genes, Dominant</term>
<term>Genes, Reporter</term>
<term>Glycosylation</term>
<term>Humans</term>
<term>Hydrogen-Ion Concentration</term>
<term>Leucine (chemistry)</term>
<term>Leukocytes, Mononuclear (metabolism)</term>
<term>Ligands</term>
<term>Luciferases (metabolism)</term>
<term>Lysosomes (chemistry)</term>
<term>Lysosomes (metabolism)</term>
<term>Macrolides (pharmacology)</term>
<term>Molecular Sequence Data</term>
<term>Mutagenesis, Site-Directed</term>
<term>Mutation</term>
<term>NF-kappa B (metabolism)</term>
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<term>Receptors, IgG (chemistry)</term>
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<term>Sequence Homology, Amino Acid</term>
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<term>Time Factors</term>
<term>Toll-Like Receptor 3 (chemistry)</term>
<term>Toll-Like Receptor 3 (metabolism)</term>
<term>Transfection</term>
<term>Tyrosine (chemistry)</term>
<term>U937 Cells</term>
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<term>Cysteine</term>
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<term>Receptors, IgG</term>
<term>Recombinant Fusion Proteins</term>
<term>Toll-Like Receptor 3</term>
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<term>Luciferases</term>
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<term>Recombinant Fusion Proteins</term>
<term>Toll-Like Receptor 3</term>
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<term>Macrolides</term>
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<term>Phagosomes</term>
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<term>Dendritic Cells</term>
<term>Endosomes</term>
<term>Leukocytes, Mononuclear</term>
<term>Lysosomes</term>
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<term>Cell Separation</term>
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<term>Flow Cytometry</term>
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<term>Time Factors</term>
<term>Transfection</term>
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<front><div type="abstract" xml:lang="en">Studies involving Toll-like receptor 3 (TLR3)-deficient mice suggest that this receptor binds double-stranded RNA. In the present study, we analyzed ligand/receptor interactions and receptor-proximal events leading to TLR3 activation. The mutagenesis approach showed that certain cysteine residues and glycosylation in TLR3 amino-terminal leucine-rich repeats were necessary for ligand-induced signaling. Furthermore, inactive mutants had a dominant negative effect, suggesting that the signaling module is a multimer. We constructed a chimeric molecule fusing the amino-terminal ectodomain of TLR3 to the transmembrane and carboxyl terminal domains of CD32a containing an immunoreceptor tyrosine-based motif. Expression of TLR3-CD32 in HEK293T cells and the myeloid cell line U937 resulted in surface localization of the receptor, whereas the nonrecombinant molecule was intracellularly localized. The synthetic double-stranded RNAs poly(I-C) and poly(A-U) induced calcium mobilization in a TLR3-CD32 stably transfected U937 clone but not in control cells transfected with other constructs. An anti-TLR3 antibody also induced Ca(2+) flux but only when cross-linked by a secondary anti-immunoglobulin antibody, confirming that multimerization by the ligand is a requirement for signaling. The inhibitors of lysosome maturation, bafilomycin and chloroquine, inhibited the poly(I-C)-induced biological response in immune cells, showing that TLR3 interacted with its ligand in acidic subcellular compartments. Furthermore, TLR3-CD32 activation with poly(I-C) was only observed within a narrow pH window (pH 5.7-6.7), whereas anti-TLR3-mediated Ca(2+) flux was pH-insensitive. The importance of an acidic pH for TLR3-ligand interaction becomes critical when using oligomeric poly(I-C) (15-40-mers). These observations demonstrate that engagement of TLR3 by poly(I-C) at an acidic pH, probably in early phagolysosomes or endosomes, induces receptor aggregation leading to signaling.</div>
</front>
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<ArticleTitle>Recognition of double-stranded RNA by human toll-like receptor 3 and downstream receptor signaling requires multimerization and an acidic pH.</ArticleTitle>
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<Abstract><AbstractText>Studies involving Toll-like receptor 3 (TLR3)-deficient mice suggest that this receptor binds double-stranded RNA. In the present study, we analyzed ligand/receptor interactions and receptor-proximal events leading to TLR3 activation. The mutagenesis approach showed that certain cysteine residues and glycosylation in TLR3 amino-terminal leucine-rich repeats were necessary for ligand-induced signaling. Furthermore, inactive mutants had a dominant negative effect, suggesting that the signaling module is a multimer. We constructed a chimeric molecule fusing the amino-terminal ectodomain of TLR3 to the transmembrane and carboxyl terminal domains of CD32a containing an immunoreceptor tyrosine-based motif. Expression of TLR3-CD32 in HEK293T cells and the myeloid cell line U937 resulted in surface localization of the receptor, whereas the nonrecombinant molecule was intracellularly localized. The synthetic double-stranded RNAs poly(I-C) and poly(A-U) induced calcium mobilization in a TLR3-CD32 stably transfected U937 clone but not in control cells transfected with other constructs. An anti-TLR3 antibody also induced Ca(2+) flux but only when cross-linked by a secondary anti-immunoglobulin antibody, confirming that multimerization by the ligand is a requirement for signaling. The inhibitors of lysosome maturation, bafilomycin and chloroquine, inhibited the poly(I-C)-induced biological response in immune cells, showing that TLR3 interacted with its ligand in acidic subcellular compartments. Furthermore, TLR3-CD32 activation with poly(I-C) was only observed within a narrow pH window (pH 5.7-6.7), whereas anti-TLR3-mediated Ca(2+) flux was pH-insensitive. The importance of an acidic pH for TLR3-ligand interaction becomes critical when using oligomeric poly(I-C) (15-40-mers). These observations demonstrate that engagement of TLR3 by poly(I-C) at an acidic pH, probably in early phagolysosomes or endosomes, induces receptor aggregation leading to signaling.</AbstractText>
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<AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>de Bouteiller</LastName>
<ForeName>Odette</ForeName>
<Initials>O</Initials>
<AffiliationInfo><Affiliation>Laboratory for Immunological Research, Schering-Plough Research Institute, 27 Chemin des Peupliers, 69571 Dardilly Cedex, France.</Affiliation>
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<Author ValidYN="Y"><LastName>Merck</LastName>
<ForeName>Estelle</ForeName>
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<Author ValidYN="Y"><LastName>Hasan</LastName>
<ForeName>Uzma A</ForeName>
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<ForeName>Sylvain</ForeName>
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<ForeName>Giorgio</ForeName>
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<Author ValidYN="Y"><LastName>Bates</LastName>
<ForeName>Elizabeth E M</ForeName>
<Initials>EE</Initials>
</Author>
<Author ValidYN="Y"><LastName>Caux</LastName>
<ForeName>Christophe</ForeName>
<Initials>C</Initials>
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