Molecular dissection of plasmacytoid dendritic cell activation in vivo during a viral infection
Plasmacytoid dendritic cells (pDC) are the major source of type I interferons (IFN‐I) during viral infections, in response to triggering of endosomal Toll‐like receptors (TLRs) 7 or 9 by viral single‐stranded RNA or unmethylated CpG DNA, respectively. Synthetic ligands have been used to disentangle...
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| Published in | The EMBO journal Vol. 37; no. 19 |
|---|---|
| Main Authors | , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
01.10.2018
Springer Nature B.V EMBO Press John Wiley and Sons Inc |
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| Online Access | Get full text |
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| Abstract | Plasmacytoid dendritic cells (pDC) are the major source of type I interferons (IFN‐I) during viral infections, in response to triggering of endosomal Toll‐like receptors (TLRs) 7 or 9 by viral single‐stranded RNA or unmethylated CpG DNA, respectively. Synthetic ligands have been used to disentangle the underlying signaling pathways. The adaptor protein AP3 is necessary to transport molecular complexes of TLRs, synthetic CpG DNA, and MyD88 into endosomal compartments allowing interferon regulatory factor 7 (IRF7) recruitment whose phosphorylation then initiates IFN‐I production. High basal expression of IRF7 by pDC and its further enhancement by positive IFN‐I feedback signaling appear to be necessary for robust cytokine production. In contrast, we show here that
in vivo
during mouse cytomegalovirus (MCMV) infection pDC produce high amounts of IFN‐I downstream of the TLR9‐to‐MyD88‐to‐IRF7 signaling pathway without requiring IFN‐I positive feedback, high IRF7 expression, or AP3‐driven endosomal routing of TLRs. Hence, the current model of the molecular requirements for professional IFN‐I production by pDC, established by using synthetic TLR ligands, does not strictly apply to a physiological viral infection.
Synopsis
In vivo
production of IFN‐I by pDC requires TLR9‐to‐MyD88‐to‐IRF7 signaling both during MCMV infection and CpG injection but IFN‐I positive feedback and AP3 function only for CpG. Hence, distinct mechanisms tune pDC responses to TLR9 triggering by synthetic ligands versus a viral infection.
TLR, IFN‐I and IFN‐γ differentially contribute to pDC activation during MCMV infection, driving largely distinct gene expression programs.
During MCMV infection but not CpG injection, pDC can produce IFN‐I
in vivo
independently of IFN‐I positive feedback and AP3‐mediated routing.
IRF7 is necessary for IFN‐I production by pDC, but low amounts are sufficient to endow them with this function.
Cell‐intrinsic LFA‐1 functions and hence cell‐cell interactions promote pDC cytokine production both during MCMV infection and CpG injection, but their precise nature remains unknown.
Graphical Abstract
Physiological settings for studying activation of interferon‐producing pDCs reveal dispensability of high basal IRF7 expression and positive IFN‐I feedback signals previously implicated based on testing with synthetic ligands. |
|---|---|
| AbstractList | Plasmacytoid dendritic cells (pDC) are the major source of type I interferons (IFN‐I) during viral infections, in response to triggering of endosomal Toll‐like receptors (TLRs) 7 or 9 by viral single‐stranded RNA or unmethylated CpG DNA, respectively. Synthetic ligands have been used to disentangle the underlying signaling pathways. The adaptor protein AP3 is necessary to transport molecular complexes of TLRs, synthetic CpG DNA, and MyD88 into endosomal compartments allowing interferon regulatory factor 7 (IRF7) recruitment whose phosphorylation then initiates IFN‐I production. High basal expression of IRF7 by pDC and its further enhancement by positive IFN‐I feedback signaling appear to be necessary for robust cytokine production. In contrast, we show here that in vivo during mouse cytomegalovirus (MCMV) infection pDC produce high amounts of IFN‐I downstream of the TLR9‐to‐MyD88‐to‐IRF7 signaling pathway without requiring IFN‐I positive feedback, high IRF7 expression, or AP3‐driven endosomal routing of TLRs. Hence, the current model of the molecular requirements for professional IFN‐I production by pDC, established by using synthetic TLR ligands, does not strictly apply to a physiological viral infection.
Synopsis
In vivo production of IFN‐I by pDC requires TLR9‐to‐MyD88‐to‐IRF7 signaling both during MCMV infection and CpG injection but IFN‐I positive feedback and AP3 function only for CpG. Hence, distinct mechanisms tune pDC responses to TLR9 triggering by synthetic ligands versus a viral infection.
TLR, IFN‐I and IFN‐γ differentially contribute to pDC activation during MCMV infection, driving largely distinct gene expression programs.
During MCMV infection but not CpG injection, pDC can produce IFN‐I in vivo independently of IFN‐I positive feedback and AP3‐mediated routing.
IRF7 is necessary for IFN‐I production by pDC, but low amounts are sufficient to endow them with this function.
Cell‐intrinsic LFA‐1 functions and hence cell‐cell interactions promote pDC cytokine production both during MCMV infection and CpG injection, but their precise nature remains unknown.
Physiological settings for studying activation of interferon‐producing pDCs reveal dispensability of high basal IRF7 expression and positive IFN‐I feedback signals previously implicated based on testing with synthetic ligands. Plasmacytoid dendritic cells (pDC) are the major source of type I interferons (IFN‐I) during viral infections, in response to triggering of endosomal Toll‐like receptors (TLRs) 7 or 9 by viral single‐stranded RNA or unmethylated CpG DNA, respectively. Synthetic ligands have been used to disentangle the underlying signaling pathways. The adaptor protein AP3 is necessary to transport molecular complexes of TLRs, synthetic CpG DNA, and MyD88 into endosomal compartments allowing interferon regulatory factor 7 (IRF7) recruitment whose phosphorylation then initiates IFN‐I production. High basal expression of IRF7 by pDC and its further enhancement by positive IFN‐I feedback signaling appear to be necessary for robust cytokine production. In contrast, we show here that in vivo during mouse cytomegalovirus (MCMV) infection pDC produce high amounts of IFN‐I downstream of the TLR9‐to‐MyD88‐to‐IRF7 signaling pathway without requiring IFN‐I positive feedback, high IRF7 expression, or AP3‐driven endosomal routing of TLRs. Hence, the current model of the molecular requirements for professional IFN‐I production by pDC, established by using synthetic TLR ligands, does not strictly apply to a physiological viral infection. Plasmacytoid dendritic cells ( pDC ) are the major source of type I interferons ( IFN ‐I) during viral infections, in response to triggering of endosomal Toll‐like receptors ( TLR s) 7 or 9 by viral single‐stranded RNA or unmethylated CpG DNA , respectively. Synthetic ligands have been used to disentangle the underlying signaling pathways. The adaptor protein AP 3 is necessary to transport molecular complexes of TLR s, synthetic CpG DNA , and MyD88 into endosomal compartments allowing interferon regulatory factor 7 ( IRF 7) recruitment whose phosphorylation then initiates IFN ‐I production. High basal expression of IRF 7 by pDC and its further enhancement by positive IFN ‐I feedback signaling appear to be necessary for robust cytokine production. In contrast, we show here that in vivo during mouse cytomegalovirus ( MCMV ) infection pDC produce high amounts of IFN ‐I downstream of the TLR 9‐to‐MyD88‐to‐ IRF 7 signaling pathway without requiring IFN ‐I positive feedback, high IRF 7 expression, or AP 3‐driven endosomal routing of TLR s. Hence, the current model of the molecular requirements for professional IFN ‐I production by pDC , established by using synthetic TLR ligands, does not strictly apply to a physiological viral infection. Plasmacytoid dendritic cells (pDC) are the major source of type I interferons (IFN-I) during viral infections, in response to triggering of endosomal Toll-like receptors (TLRs) 7 or 9 by viral single-stranded RNA or unmethylated CpG DNA, respectively. Synthetic ligands have been used to disentangle the underlying signaling pathways. The adaptor protein AP3 is necessary to transport molecular complexes of TLRs, synthetic CpG DNA, and MyD88 into endosomal compartments allowing interferon regulatory factor 7 (IRF7) recruitment whose phosphorylation then initiates IFN-I production. High basal expression of IRF7 by pDC and its further enhancement by positive IFN-I feedback signaling appear to be necessary for robust cytokine production. In contrast, we show here that during mouse cytomegalovirus (MCMV) infection pDC produce high amounts of IFN-I downstream of the TLR9-to-MyD88-to-IRF7 signaling pathway without requiring IFN-I positive feedback, high IRF7 expression, or AP3-driven endosomal routing of TLRs. Hence, the current model of the molecular requirements for professional IFN-I production by pDC, established by using synthetic TLR ligands, does not strictly apply to a physiological viral infection. Plasmacytoid dendritic cells (pDC) are the major source of type I interferons (IFN‐I) during viral infections, in response to triggering of endosomal Toll‐like receptors (TLRs) 7 or 9 by viral single‐stranded RNA or unmethylated CpG DNA, respectively. Synthetic ligands have been used to disentangle the underlying signaling pathways. The adaptor protein AP3 is necessary to transport molecular complexes of TLRs, synthetic CpG DNA, and MyD88 into endosomal compartments allowing interferon regulatory factor 7 (IRF7) recruitment whose phosphorylation then initiates IFN‐I production. High basal expression of IRF7 by pDC and its further enhancement by positive IFN‐I feedback signaling appear to be necessary for robust cytokine production. In contrast, we show here that in vivo during mouse cytomegalovirus (MCMV) infection pDC produce high amounts of IFN‐I downstream of the TLR9‐to‐MyD88‐to‐IRF7 signaling pathway without requiring IFN‐I positive feedback, high IRF7 expression, or AP3‐driven endosomal routing of TLRs. Hence, the current model of the molecular requirements for professional IFN‐I production by pDC, established by using synthetic TLR ligands, does not strictly apply to a physiological viral infection. Synopsis In vivo production of IFN‐I by pDC requires TLR9‐to‐MyD88‐to‐IRF7 signaling both during MCMV infection and CpG injection but IFN‐I positive feedback and AP3 function only for CpG. Hence, distinct mechanisms tune pDC responses to TLR9 triggering by synthetic ligands versus a viral infection. TLR, IFN‐I and IFN‐γ differentially contribute to pDC activation during MCMV infection, driving largely distinct gene expression programs. During MCMV infection but not CpG injection, pDC can produce IFN‐I in vivo independently of IFN‐I positive feedback and AP3‐mediated routing. IRF7 is necessary for IFN‐I production by pDC, but low amounts are sufficient to endow them with this function. Cell‐intrinsic LFA‐1 functions and hence cell‐cell interactions promote pDC cytokine production both during MCMV infection and CpG injection, but their precise nature remains unknown. Graphical Abstract Physiological settings for studying activation of interferon‐producing pDCs reveal dispensability of high basal IRF7 expression and positive IFN‐I feedback signals previously implicated based on testing with synthetic ligands. Plasmacytoid dendritic cells (pDC) are the major source of type I interferons (IFN-I) during viral infections, in response to triggering of endosomal Toll-like receptors (TLRs) 7 or 9 by viral single-stranded RNA or unmethylated CpG DNA, respectively. Synthetic ligands have been used to disentangle the underlying signaling pathways. The adaptor protein AP3 is necessary to transport molecular complexes of TLRs, synthetic CpG DNA, and MyD88 into endosomal compartments allowing interferon regulatory factor 7 (IRF7) recruitment whose phosphorylation then initiates IFN-I production. High basal expression of IRF7 by pDC and its further enhancement by positive IFN-I feedback signaling appear to be necessary for robust cytokine production. In contrast, we show here that in vivo during mouse cytomegalovirus (MCMV) infection pDC produce high amounts of IFN-I downstream of the TLR9-to-MyD88-to-IRF7 signaling pathway without requiring IFN-I positive feedback, high IRF7 expression, or AP3-driven endosomal routing of TLRs. Hence, the current model of the molecular requirements for professional IFN-I production by pDC, established by using synthetic TLR ligands, does not strictly apply to a physiological viral infection.Plasmacytoid dendritic cells (pDC) are the major source of type I interferons (IFN-I) during viral infections, in response to triggering of endosomal Toll-like receptors (TLRs) 7 or 9 by viral single-stranded RNA or unmethylated CpG DNA, respectively. Synthetic ligands have been used to disentangle the underlying signaling pathways. The adaptor protein AP3 is necessary to transport molecular complexes of TLRs, synthetic CpG DNA, and MyD88 into endosomal compartments allowing interferon regulatory factor 7 (IRF7) recruitment whose phosphorylation then initiates IFN-I production. High basal expression of IRF7 by pDC and its further enhancement by positive IFN-I feedback signaling appear to be necessary for robust cytokine production. In contrast, we show here that in vivo during mouse cytomegalovirus (MCMV) infection pDC produce high amounts of IFN-I downstream of the TLR9-to-MyD88-to-IRF7 signaling pathway without requiring IFN-I positive feedback, high IRF7 expression, or AP3-driven endosomal routing of TLRs. Hence, the current model of the molecular requirements for professional IFN-I production by pDC, established by using synthetic TLR ligands, does not strictly apply to a physiological viral infection. |
| Author | Chelbi, Rabie Pollet, Emeline Abbas, Abdenour Lawrence, Toby Pierre, Philippe Naciri, Karima Bessou, Gilles Tomasello, Elena Vu Manh, Thien‐Phong Fries, Anissa Dalod, Marc Gressier, Elise |
| AuthorAffiliation | 3 Present address: Department of Microbiology and Immunology Peter Doherty Institute for Infection and Immunity The University of Melbourne Parkville Vic. Australia 1 Aix Marseille Univ CNRS INSERM CIML Centre d'Immunologie de Marseille‐Luminy Marseille France 2 Present address: Department of Dermatology University Hospital CHUV Lausanne Switzerland |
| AuthorAffiliation_xml | – name: 2 Present address: Department of Dermatology University Hospital CHUV Lausanne Switzerland – name: 3 Present address: Department of Microbiology and Immunology Peter Doherty Institute for Infection and Immunity The University of Melbourne Parkville Vic. Australia – name: 1 Aix Marseille Univ CNRS INSERM CIML Centre d'Immunologie de Marseille‐Luminy Marseille France |
| Author_xml | – sequence: 1 givenname: Elena surname: Tomasello fullname: Tomasello, Elena email: tomasell@ciml.univ-mrs.fr organization: Aix Marseille Univ, CNRS, INSERM, CIML, Centre d'Immunologie de Marseille‐Luminy – sequence: 2 givenname: Karima surname: Naciri fullname: Naciri, Karima organization: Aix Marseille Univ, CNRS, INSERM, CIML, Centre d'Immunologie de Marseille‐Luminy – sequence: 3 givenname: Rabie surname: Chelbi fullname: Chelbi, Rabie organization: Aix Marseille Univ, CNRS, INSERM, CIML, Centre d'Immunologie de Marseille‐Luminy – sequence: 4 givenname: Gilles surname: Bessou fullname: Bessou, Gilles organization: Aix Marseille Univ, CNRS, INSERM, CIML, Centre d'Immunologie de Marseille‐Luminy – sequence: 5 givenname: Anissa surname: Fries fullname: Fries, Anissa organization: Aix Marseille Univ, CNRS, INSERM, CIML, Centre d'Immunologie de Marseille‐Luminy, Department of Dermatology, University Hospital CHUV – sequence: 6 givenname: Elise surname: Gressier fullname: Gressier, Elise organization: Aix Marseille Univ, CNRS, INSERM, CIML, Centre d'Immunologie de Marseille‐Luminy, Department of Microbiology and Immunology, Peter Doherty Institute for Infection and Immunity, The University of Melbourne – sequence: 7 givenname: Abdenour surname: Abbas fullname: Abbas, Abdenour organization: Aix Marseille Univ, CNRS, INSERM, CIML, Centre d'Immunologie de Marseille‐Luminy – sequence: 8 givenname: Emeline surname: Pollet fullname: Pollet, Emeline organization: Aix Marseille Univ, CNRS, INSERM, CIML, Centre d'Immunologie de Marseille‐Luminy – sequence: 9 givenname: Philippe orcidid: 0000-0003-0863-8255 surname: Pierre fullname: Pierre, Philippe organization: Aix Marseille Univ, CNRS, INSERM, CIML, Centre d'Immunologie de Marseille‐Luminy – sequence: 10 givenname: Toby surname: Lawrence fullname: Lawrence, Toby organization: Aix Marseille Univ, CNRS, INSERM, CIML, Centre d'Immunologie de Marseille‐Luminy – sequence: 11 givenname: Thien‐Phong surname: Vu Manh fullname: Vu Manh, Thien‐Phong organization: Aix Marseille Univ, CNRS, INSERM, CIML, Centre d'Immunologie de Marseille‐Luminy – sequence: 12 givenname: Marc orcidid: 0000-0002-6436-7966 surname: Dalod fullname: Dalod, Marc email: dalod@ciml.univ-mrs.fr organization: Aix Marseille Univ, CNRS, INSERM, CIML, Centre d'Immunologie de Marseille‐Luminy |
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| ISSN | 0261-4189 1460-2075 |
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| Issue | 19 |
| Keywords | IRF7 plasmacytoid dendritic cells viral infection mouse cytomegalovirus type I interferons Virology & Host Pathogen Interaction Microbiology viral infection Subject Categories Immunology |
| Language | English |
| License | Attribution 2018 The Authors. Published under the terms of the CC BY NC ND 4.0 license. Attribution - NonCommercial - NoDerivatives: http://creativecommons.org/licenses/by-nc-nd This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made. |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 These authors contributed equally to this work These authors contributed equally to this work as senior authors |
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| OpenAccessLink | https://onlinelibrary.wiley.com/doi/abs/10.15252%2Fembj.201798836 |
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| Snippet | Plasmacytoid dendritic cells (pDC) are the major source of type I interferons (IFN‐I) during viral infections, in response to triggering of endosomal Toll‐like... Plasmacytoid dendritic cells (pDC) are the major source of type I interferons (IFN-I) during viral infections, in response to triggering of endosomal Toll-like... Plasmacytoid dendritic cells ( pDC ) are the major source of type I interferons ( IFN ‐I) during viral infections, in response to triggering of endosomal... |
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| SubjectTerms | Cell activation Cell interactions CpG islands Cytokines Cytomegalovirus Dendritic cells Deoxyribonucleic acid DNA EMBO19 EMBO23 Feedback Gene expression Immune system Immunology Infections Injection Interferon Interferon regulatory factor Interferon regulatory factor 7 IRF7 Life Sciences Ligands mouse cytomegalovirus MyD88 protein Phosphorylation plasmacytoid dendritic cells Positive feedback Proteins Receptors Ribonucleic acid RNA Signal transduction Signaling TLR9 protein Toll-like receptors type I interferons viral infection Viral infections |
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| Title | Molecular dissection of plasmacytoid dendritic cell activation in vivo during a viral infection |
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