Unified polymerization mechanism for the assembly of ASC-dependent inflammasomes
Inflammasomes elicit host defense inside cells by activating caspase-1 for cytokine maturation and cell death. AIM2 and NLRP3 are representative sensor proteins in two major families of inflammasomes. The adaptor protein ASC bridges the sensor proteins and caspase-1 to form ternary inflammasome comp...
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| Published in: | Cell Vol. 156; no. 6; p. 1193 |
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| Main Authors: | , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
| Published: |
United States
13.03.2014
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| Subjects: | |
| ISSN: | 1097-4172, 1097-4172 |
| Online Access: | Get more information |
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| Abstract | Inflammasomes elicit host defense inside cells by activating caspase-1 for cytokine maturation and cell death. AIM2 and NLRP3 are representative sensor proteins in two major families of inflammasomes. The adaptor protein ASC bridges the sensor proteins and caspase-1 to form ternary inflammasome complexes, achieved through pyrin domain (PYD) interactions between sensors and ASC and through caspase activation and recruitment domain (CARD) interactions between ASC and caspase-1. We found that PYD and CARD both form filaments. Activated AIM2 and NLRP3 nucleate PYD filaments of ASC, which, in turn, cluster the CARD of ASC. ASC thus nucleates CARD filaments of caspase-1, leading to proximity-induced activation. Endogenous NLRP3 inflammasome is also filamentous. The cryoelectron microscopy structure of ASC(PYD) filament at near-atomic resolution provides a template for homo- and hetero-PYD/PYD associations, as confirmed by structure-guided mutagenesis. We propose that ASC-dependent inflammasomes in both families share a unified assembly mechanism that involves two successive steps of nucleation-induced polymerization. PAPERFLICK: |
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| AbstractList | Inflammasomes elicit host defense inside cells by activating caspase-1 for cytokine maturation and cell death. AIM2 and NLRP3 are representative sensor proteins in two major families of inflammasomes. The adaptor protein ASC bridges the sensor proteins and caspase-1 to form ternary inflammasome complexes, achieved through pyrin domain (PYD) interactions between sensors and ASC and through caspase activation and recruitment domain (CARD) interactions between ASC and caspase-1. We found that PYD and CARD both form filaments. Activated AIM2 and NLRP3 nucleate PYD filaments of ASC, which, in turn, cluster the CARD of ASC. ASC thus nucleates CARD filaments of caspase-1, leading to proximity-induced activation. Endogenous NLRP3 inflammasome is also filamentous. The cryoelectron microscopy structure of ASC(PYD) filament at near-atomic resolution provides a template for homo- and hetero-PYD/PYD associations, as confirmed by structure-guided mutagenesis. We propose that ASC-dependent inflammasomes in both families share a unified assembly mechanism that involves two successive steps of nucleation-induced polymerization. PAPERFLICK:Inflammasomes elicit host defense inside cells by activating caspase-1 for cytokine maturation and cell death. AIM2 and NLRP3 are representative sensor proteins in two major families of inflammasomes. The adaptor protein ASC bridges the sensor proteins and caspase-1 to form ternary inflammasome complexes, achieved through pyrin domain (PYD) interactions between sensors and ASC and through caspase activation and recruitment domain (CARD) interactions between ASC and caspase-1. We found that PYD and CARD both form filaments. Activated AIM2 and NLRP3 nucleate PYD filaments of ASC, which, in turn, cluster the CARD of ASC. ASC thus nucleates CARD filaments of caspase-1, leading to proximity-induced activation. Endogenous NLRP3 inflammasome is also filamentous. The cryoelectron microscopy structure of ASC(PYD) filament at near-atomic resolution provides a template for homo- and hetero-PYD/PYD associations, as confirmed by structure-guided mutagenesis. We propose that ASC-dependent inflammasomes in both families share a unified assembly mechanism that involves two successive steps of nucleation-induced polymerization. PAPERFLICK: Inflammasomes elicit host defense inside cells by activating caspase-1 for cytokine maturation and cell death. AIM2 and NLRP3 are representative sensor proteins in two major families of inflammasomes. The adaptor protein ASC bridges the sensor proteins and caspase-1 to form ternary inflammasome complexes, achieved through pyrin domain (PYD) interactions between sensors and ASC and through caspase activation and recruitment domain (CARD) interactions between ASC and caspase-1. We found that PYD and CARD both form filaments. Activated AIM2 and NLRP3 nucleate PYD filaments of ASC, which, in turn, cluster the CARD of ASC. ASC thus nucleates CARD filaments of caspase-1, leading to proximity-induced activation. Endogenous NLRP3 inflammasome is also filamentous. The cryoelectron microscopy structure of ASC(PYD) filament at near-atomic resolution provides a template for homo- and hetero-PYD/PYD associations, as confirmed by structure-guided mutagenesis. We propose that ASC-dependent inflammasomes in both families share a unified assembly mechanism that involves two successive steps of nucleation-induced polymerization. PAPERFLICK: |
| Author | Atianand, Maninjay K Wu, Hao Yin, Qian Vos, Matthijn R Schröder, Gunnar F Ruan, Jianbin Egelman, Edward H Magupalli, Venkat Giri Lu, Alvin Fitzgerald, Katherine A |
| Author_xml | – sequence: 1 givenname: Alvin surname: Lu fullname: Lu, Alvin organization: Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, MA 02115, USA; Program in Cellular and Molecular Medicine, Boston Children's Hospital, Boston, MA 02115, USA – sequence: 2 givenname: Venkat Giri surname: Magupalli fullname: Magupalli, Venkat Giri organization: Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, MA 02115, USA; Program in Cellular and Molecular Medicine, Boston Children's Hospital, Boston, MA 02115, USA – sequence: 3 givenname: Jianbin surname: Ruan fullname: Ruan, Jianbin organization: Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, MA 02115, USA; Program in Cellular and Molecular Medicine, Boston Children's Hospital, Boston, MA 02115, USA – sequence: 4 givenname: Qian surname: Yin fullname: Yin, Qian organization: Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, MA 02115, USA; Program in Cellular and Molecular Medicine, Boston Children's Hospital, Boston, MA 02115, USA – sequence: 5 givenname: Maninjay K surname: Atianand fullname: Atianand, Maninjay K organization: Division of Infectious Diseases and Immunology, Department of Medicine, University of Massachusetts Medical School, Worcester, MA 01655, USA – sequence: 6 givenname: Matthijn R surname: Vos fullname: Vos, Matthijn R organization: FEI Company, Nanoport Europe, 5651 GG Eindhoven, the Netherlands – sequence: 7 givenname: Gunnar F surname: Schröder fullname: Schröder, Gunnar F organization: Institute of Complex Systems, Forschungszentrum Jülich, 52425 Jülich, Germany; Physics Department, Heinrich-Heine Universität Düsseldorf, 40225 Düsseldorf, Germany – sequence: 8 givenname: Katherine A surname: Fitzgerald fullname: Fitzgerald, Katherine A organization: Division of Infectious Diseases and Immunology, Department of Medicine, University of Massachusetts Medical School, Worcester, MA 01655, USA – sequence: 9 givenname: Hao surname: Wu fullname: Wu, Hao email: hao.wu@childrens.harvard.edu organization: Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, MA 02115, USA; Program in Cellular and Molecular Medicine, Boston Children's Hospital, Boston, MA 02115, USA. Electronic address: hao.wu@childrens.harvard.edu – sequence: 10 givenname: Edward H surname: Egelman fullname: Egelman, Edward H organization: Department of Biochemistry and Molecular Genetics, University of Virginia, Charlottesville, VA 22908, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/24630722$$D View this record in MEDLINE/PubMed |
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| Snippet | Inflammasomes elicit host defense inside cells by activating caspase-1 for cytokine maturation and cell death. AIM2 and NLRP3 are representative sensor... |
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| SubjectTerms | Amino Acid Sequence CARD Signaling Adaptor Proteins Carrier Proteins - metabolism Cryoelectron Microscopy Cytoskeletal Proteins - chemistry Cytoskeletal Proteins - metabolism DNA-Binding Proteins Humans Inflammasomes - chemistry Inflammasomes - metabolism Inflammasomes - ultrastructure Interleukin-1beta - metabolism Models, Molecular Molecular Sequence Data NLR Family, Pyrin Domain-Containing 3 Protein Nuclear Proteins - metabolism Polymerization Protein Structure, Tertiary |
| Title | Unified polymerization mechanism for the assembly of ASC-dependent inflammasomes |
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