The innate immune sensor NLRC3 attenuates Toll-like receptor signaling via modification of the signaling adaptor TRAF6 and transcription factor NF-κB
Sensors of the NLR family generally activate innate immunity. Ting et al ., however, demonstrate that the little-known NLRC3 negatively regulates Toll-like receptor signaling by altering ubiquitination of the signaling adaptor TRAF6. Several members of the NLR family of sensors activate innate immun...
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| Published in | Nature immunology Vol. 13; no. 9; pp. 823 - 831 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
New York
Nature Publishing Group US
01.09.2012
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Sensors of the NLR family generally activate innate immunity. Ting
et al
., however, demonstrate that the little-known NLRC3 negatively regulates Toll-like receptor signaling by altering ubiquitination of the signaling adaptor TRAF6.
Several members of the NLR family of sensors activate innate immunity. In contrast, we found here that NLRC3 inhibited Toll-like receptor (TLR)-dependent activation of the transcription factor NF-κB by interacting with the TLR signaling adaptor TRAF6 to attenuate Lys63 (K63)-linked ubiquitination of TRAF6 and activation of NF-κB. We used bioinformatics to predict interactions between NLR and TRAF proteins, including interactions of TRAF with NLRC3.
In vivo
, macrophage expression of
Nlrc3
mRNA was diminished by the administration of lipopolysaccharide (LPS) but was restored when cellular activation subsided. To assess biologic relevance, we generated
Nlrc3
−/−
mice. LPS-treated
Nlrc3
−/−
macrophages had more K63-ubiquitinated TRAF6, nuclear NF-κB and proinflammatory cytokines. Finally, LPS-treated
Nlrc3
−/−
mice had more signs of inflammation. Thus, signaling via NLRC3 and TLR constitutes a negative feedback loop. Furthermore, prevalent NLR-TRAF interactions suggest the formation of a 'TRAFasome' complex. |
|---|---|
| AbstractList | Several members of the NLR family of sensors activate innate immunity. In contrast, we found here that NLRC3 inhibited Toll-like receptor (TLR)-dependent activation of the transcription factor NF-κB by interacting with the TLR signaling adaptor TRAF6 to attenuate Lys63 (K63)-linked ubiquitination of TRAF6 and activation of NF-κB. We used bioinformatics to predict interactions between NLR and TRAF proteins, including interactions of TRAF with NLRC3. In vivo, macrophage expression of Nlrc3 mRNA was diminished by the administration of lipopolysaccharide (LPS) but was restored when cellular activation subsided. To assess biologic relevance, we generated Nlrc3(-/-) mice. LPS-treated Nlrc3(-/-) macrophages had more K63-ubiquitinated TRAF6, nuclear NF-κB and proinflammatory cytokines. Finally, LPS-treated Nlrc3(-/-) mice had more signs of inflammation. Thus, signaling via NLRC3 and TLR constitutes a negative feedback loop. Furthermore, prevalent NLR-TRAF interactions suggest the formation of a 'TRAFasome' complex. Several members of the NLR family of sensors activate innate immunity. In contrast, we found here that NLRC3 inhibited Toll-like receptor (TLR)-dependent activation of the transcription factor NF- Kappa B by interacting with the TLR signaling adaptor TRAF6 to attenuate Lys63 (K63)-linked ubiquitination of TRAF6 and activation of NF- Kappa B. We used bioinformatics to predict interactions between NLR and TRAF proteins, including interactions of TRAF with NLRC3. In vivo, macrophage expression of Nlrc3 mRNA was diminished by the administration of lipopolysaccharide (LPS) but was restored when cellular activation subsided. To assess biologic relevance, we generated Nlrc3 super(-/-) mice. LPS-treated Nlrc3 super(-/-) macrophages had more K63-ubiquitinated TRAF6, nuclear NF- Kappa B and proinflammatory cytokines. Finally, LPS-treated Nlrc3 super(-/-) mice had more signs of inflammation. Thus, signaling via NLRC3 and TLR constitutes a negative feedback loop. Furthermore, prevalent NLR-TRAF interactions suggest the formation of a 'TRAFasome' complex. Several members of the NLR family of sensors activate innate immunity. In contrast, we found here that NLRC3 inhibited Toll-like receptor (TLR)-dependent activation of the transcription factor NF-κB by interacting with the TLR signaling adaptor TRAF6 to attenuate Lys63 (K63)-linked ubiquitination of TRAF6 and activation of NF-κB. We used bioinformatics to predict interactions between NLR and TRAF proteins, including interactions of TRAF with NLRC3. In vivo, macrophage expression of N/rc3 mRNA was diminished by the administration of lipopolysaccharide (LPS) but was restored when cellular activation subsided. To assess biologic relevance, we generated [Nlrc3.sup.-/-] mice. LPS-treated [Nlrc3.sup.-/-] macrophages had more K63-ubiquitinated TRAF6, nuclear NF-κB and proinflammatory cytokines. Finally, LPS-treated [Nlrc3.sup.-/-] mice had more signs of inflammation. Thus, signaling via NLRC3 and TLR constitutes a negative feedback loop. Furthermore, prevalent NLR-TRAF interactions suggest the formation of a 'TRAFasome' complex. Sensors of the NLR family generally activate innate immunity. Ting et al ., however, demonstrate that the little-known NLRC3 negatively regulates Toll-like receptor signaling by altering ubiquitination of the signaling adaptor TRAF6. Several members of the NLR family of sensors activate innate immunity. In contrast, we found here that NLRC3 inhibited Toll-like receptor (TLR)-dependent activation of the transcription factor NF-κB by interacting with the TLR signaling adaptor TRAF6 to attenuate Lys63 (K63)-linked ubiquitination of TRAF6 and activation of NF-κB. We used bioinformatics to predict interactions between NLR and TRAF proteins, including interactions of TRAF with NLRC3. In vivo , macrophage expression of Nlrc3 mRNA was diminished by the administration of lipopolysaccharide (LPS) but was restored when cellular activation subsided. To assess biologic relevance, we generated Nlrc3 −/− mice. LPS-treated Nlrc3 −/− macrophages had more K63-ubiquitinated TRAF6, nuclear NF-κB and proinflammatory cytokines. Finally, LPS-treated Nlrc3 −/− mice had more signs of inflammation. Thus, signaling via NLRC3 and TLR constitutes a negative feedback loop. Furthermore, prevalent NLR-TRAF interactions suggest the formation of a 'TRAFasome' complex. Several members of the NLR family of sensors activate innate immunity. In contrast, we found here that NLRC3 inhibited Toll-like receptor (TLR)-dependent activation of the transcription factor NF-κB by interacting with the TLR signaling adaptor TRAF6 to attenuate Lys63 (K63)-linked ubiquitination of TRAF6 and activation of NF-κB. We used bioinformatics to predict interactions between NLR and TRAF proteins, including interactions of TRAF with NLRC3. In vivo , macrophage expression of Nlrc3 mRNA was diminished by the administration of lipopolysaccharide (LPS) but was restored when cellular activation subsided. To assess biologic relevance, we generated Nlrc3 −/− mice. LPS-treated Nlrc3 −/− macrophages had more K63-ubiquitinated TRAF6, nuclear NF-κB and proinflammatory cytokines. Finally, LPS-treated Nlrc3 −/− mice had more signs of inflammation. Thus, signaling via NLRC3 and TLR constitutes a negative feedback loop. Furthermore, prevalent NLR-TRAF interactions suggest the formation of a ‘TRAFasome’ complex. |
| Audience | Academic |
| Author | Roberts, Reid A Holl, Eda K Davis, Beckley K Ting, Jenny P-Y Schneider, Monika Koller, Beverly H Eitas, Timothy K Zhang, Lu Rahman, Adeeb H Conti, Brian J Zimmermann, Albert G Swanson, Karen V Wen, Haitao Allen, Irving C Ye, Zhengmao |
| AuthorAffiliation | 5 Department of Genetics, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA 4 Center for Translational Immunology and Institute for Inflammatory Diseases, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA 3 School of Dentistry, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA 1 Department of Microbiology and Immunology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA 2 Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA |
| AuthorAffiliation_xml | – name: 1 Department of Microbiology and Immunology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA – name: 4 Center for Translational Immunology and Institute for Inflammatory Diseases, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA – name: 3 School of Dentistry, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA – name: 5 Department of Genetics, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA – name: 2 Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA |
| Author_xml | – sequence: 1 givenname: Monika surname: Schneider fullname: Schneider, Monika organization: Department of Microbiology and Immunology, University of North Carolina at Chapel Hill – sequence: 2 givenname: Albert G surname: Zimmermann fullname: Zimmermann, Albert G organization: Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill – sequence: 3 givenname: Reid A surname: Roberts fullname: Roberts, Reid A organization: Department of Microbiology and Immunology, University of North Carolina at Chapel Hill – sequence: 4 givenname: Lu surname: Zhang fullname: Zhang, Lu organization: School of Dentistry, University of North Carolina at Chapel Hill – sequence: 5 givenname: Karen V surname: Swanson fullname: Swanson, Karen V organization: Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill – sequence: 6 givenname: Haitao surname: Wen fullname: Wen, Haitao organization: Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill – sequence: 7 givenname: Beckley K surname: Davis fullname: Davis, Beckley K organization: Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill, Present addresses: Department of Biology, Franklin and Marshall College, Lancaster, Pennsylvania, USA (B.K.D.); Duke Translational Research Institute, Duke University, Durham, North Carolina, USA (E.K.H.); HIV Drug Discovery Unit, Infectious Diseases Medicines Discovery & Development, GlaxoSmithKline, Research Triangle Park, North Carolina, USA (Z.Y.); Department of Medicine, Division of Liver Diseases, Mount Sinai School of Medicine, New York, New York, USA (A.H.R.); and Department of Biochemistry and Molecular Biology, Oregon Health & Science University, Portland, Oregon, USA (B.J.C.) – sequence: 8 givenname: Irving C surname: Allen fullname: Allen, Irving C organization: Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill – sequence: 9 givenname: Eda K surname: Holl fullname: Holl, Eda K organization: Department of Microbiology and Immunology, University of North Carolina at Chapel Hill, Present addresses: Department of Biology, Franklin and Marshall College, Lancaster, Pennsylvania, USA (B.K.D.); Duke Translational Research Institute, Duke University, Durham, North Carolina, USA (E.K.H.); HIV Drug Discovery Unit, Infectious Diseases Medicines Discovery & Development, GlaxoSmithKline, Research Triangle Park, North Carolina, USA (Z.Y.); Department of Medicine, Division of Liver Diseases, Mount Sinai School of Medicine, New York, New York, USA (A.H.R.); and Department of Biochemistry and Molecular Biology, Oregon Health & Science University, Portland, Oregon, USA (B.J.C.) – sequence: 10 givenname: Zhengmao surname: Ye fullname: Ye, Zhengmao organization: Department of Microbiology and Immunology, University of North Carolina at Chapel Hill, Present addresses: Department of Biology, Franklin and Marshall College, Lancaster, Pennsylvania, USA (B.K.D.); Duke Translational Research Institute, Duke University, Durham, North Carolina, USA (E.K.H.); HIV Drug Discovery Unit, Infectious Diseases Medicines Discovery & Development, GlaxoSmithKline, Research Triangle Park, North Carolina, USA (Z.Y.); Department of Medicine, Division of Liver Diseases, Mount Sinai School of Medicine, New York, New York, USA (A.H.R.); and Department of Biochemistry and Molecular Biology, Oregon Health & Science University, Portland, Oregon, USA (B.J.C.) – sequence: 11 givenname: Adeeb H surname: Rahman fullname: Rahman, Adeeb H organization: Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill, Present addresses: Department of Biology, Franklin and Marshall College, Lancaster, Pennsylvania, USA (B.K.D.); Duke Translational Research Institute, Duke University, Durham, North Carolina, USA (E.K.H.); HIV Drug Discovery Unit, Infectious Diseases Medicines Discovery & Development, GlaxoSmithKline, Research Triangle Park, North Carolina, USA (Z.Y.); Department of Medicine, Division of Liver Diseases, Mount Sinai School of Medicine, New York, New York, USA (A.H.R.); and Department of Biochemistry and Molecular Biology, Oregon Health & Science University, Portland, Oregon, USA (B.J.C.) – sequence: 12 givenname: Brian J surname: Conti fullname: Conti, Brian J organization: Department of Microbiology and Immunology, University of North Carolina at Chapel Hill, Present addresses: Department of Biology, Franklin and Marshall College, Lancaster, Pennsylvania, USA (B.K.D.); Duke Translational Research Institute, Duke University, Durham, North Carolina, USA (E.K.H.); HIV Drug Discovery Unit, Infectious Diseases Medicines Discovery & Development, GlaxoSmithKline, Research Triangle Park, North Carolina, USA (Z.Y.); Department of Medicine, Division of Liver Diseases, Mount Sinai School of Medicine, New York, New York, USA (A.H.R.); and Department of Biochemistry and Molecular Biology, Oregon Health & Science University, Portland, Oregon, USA (B.J.C.) – sequence: 13 givenname: Timothy K surname: Eitas fullname: Eitas, Timothy K organization: Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill – sequence: 14 givenname: Beverly H surname: Koller fullname: Koller, Beverly H organization: School of Dentistry, University of North Carolina at Chapel Hill – sequence: 15 givenname: Jenny P-Y surname: Ting fullname: Ting, Jenny P-Y email: jenny_ting@med.unc.edu organization: Department of Microbiology and Immunology, University of North Carolina at Chapel Hill, Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill, Center for Translational Immunology and Institute for Inflammatory Diseases, University of North Carolina at Chapel Hill, Department of Genetics, University of North Carolina at Chapel Hill |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/22863753$$D View this record in MEDLINE/PubMed |
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| Copyright | Springer Nature America, Inc. 2012 COPYRIGHT 2012 Nature Publishing Group 2012 Nature America, Inc. All rights reserved. 2012 |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 ObjectType-Article-2 ObjectType-Feature-1 Present addresses: Department of Biology, Franklin and Marshall College, Lancaster, Pennsylvania, USA (B.K.D.); Duke Translational Research Institute, Duke University, Durham, North Carolina, USA (E.K.H.); HIV Drug Discovery Unit, Infectious Diseases Medicines Discovery & Development, GlaxoSmithKline, Research Triangle Park, North Carolina, USA (Z.Y.); Department of Medicine, Division of Liver Diseases, Mount Sinai School of Medicine, New York, New York, USA (A.H.R.); and Department of Biochemistry and Molecular Biology, Oregon Health & Science University, Portland, Oregon, USA (B.J.C.). |
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| Snippet | Sensors of the NLR family generally activate innate immunity. Ting
et al
., however, demonstrate that the little-known NLRC3 negatively regulates Toll-like... Several members of the NLR family of sensors activate innate immunity. In contrast, we found here that NLRC3 inhibited Toll-like receptor (TLR)-dependent... |
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| SubjectTerms | 631/1647/48 631/250/2502 631/250/256 631/250/516 Amino Acid Sequence Animals Biomedical and Life Sciences Biomedicine Cytokines Feedback, Physiological HEK293 Cells Humans Immunology Infectious Diseases Macrophages - immunology Macrophages - metabolism Mice Mice, Inbred C57BL Mice, Knockout Molecular Sequence Data NF-kappa B - immunology NF-kappa B - metabolism Physiological aspects Real-Time Polymerase Chain Reaction Receptors, G-Protein-Coupled - immunology Receptors, G-Protein-Coupled - metabolism Reverse Transcriptase Polymerase Chain Reaction Signal Transduction - immunology TNF Receptor-Associated Factor 6 - immunology TNF Receptor-Associated Factor 6 - metabolism Toll-like receptors Toll-Like Receptors - immunology Toll-Like Receptors - metabolism Transcription factors |
| Title | The innate immune sensor NLRC3 attenuates Toll-like receptor signaling via modification of the signaling adaptor TRAF6 and transcription factor NF-κB |
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