Inflammasome Activation Triggers Blood Clotting and Host Death through Pyroptosis
Inflammasome activation and subsequent pyroptosis are critical defense mechanisms against microbes. However, overactivation of inflammasome leads to death of the host. Although recent studies have uncovered the mechanism of pyroptosis following inflammasome activation, how pyroptotic cell death driv...
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| Published in | Immunity (Cambridge, Mass.) Vol. 50; no. 6; pp. 1401 - 1411.e4 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
18.06.2019
Elsevier Limited |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Inflammasome activation and subsequent pyroptosis are critical defense mechanisms against microbes. However, overactivation of inflammasome leads to death of the host. Although recent studies have uncovered the mechanism of pyroptosis following inflammasome activation, how pyroptotic cell death drives pathogenesis, eventually leading to death of the host, is unknown. Here, we identified inflammasome activation as a trigger for blood clotting through pyroptosis. We have shown that canonical inflammasome activation by the conserved type III secretion system (T3SS) rod proteins from Gram-negative bacteria or noncanonical inflammasome activation by lipopolysaccharide (LPS) induced systemic blood clotting and massive thrombosis in tissues. Following inflammasome activation, pyroptotic macrophages released tissue factor (TF), an essential initiator of coagulation cascades. Genetic or pharmacological inhibition of TF abolishes inflammasome-mediated blood clotting and protects against death. Our data reveal that blood clotting is the major cause of host death following inflammasome activation and demonstrate that inflammasome bridges inflammation with thrombosis.
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•Canonical or noncanonical inflammasome activation leads to blood clotting•Inflammasome activation induces blood clotting through pyroptosis•Tissue factor released from pyroptotic macrophages drives blood blotting•Interfering tissue factor prevents pyroptosis-induced lethality
Overactivation of inflammasome leads to death of the host. Wu and colleagues demonstrate that activation of coagulation is responsible for inflammasome activation-induced death. |
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| AbstractList | SummaryInflammasome activation and subsequent pyroptosis are critical defense mechanisms against microbes. However, overactivation of inflammasome leads to death of the host. Although recent studies have uncovered the mechanism of pyroptosis following inflammasome activation, how pyroptotic cell death drives pathogenesis, eventually leading to death of the host, is unknown. Here, we identified inflammasome activation as a trigger for blood clotting through pyroptosis. We have shown that canonical inflammasome activation by the conserved type III secretion system (T3SS) rod proteins from Gram-negative bacteria or noncanonical inflammasome activation by lipopolysaccharide (LPS) induced systemic blood clotting and massive thrombosis in tissues. Following inflammasome activation, pyroptotic macrophages released tissue factor (TF), an essential initiator of coagulation cascades. Genetic or pharmacological inhibition of TF abolishes inflammasome-mediated blood clotting and protects against death. Our data reveal that blood clotting is the major cause of host death following inflammasome activation and demonstrate that inflammasome bridges inflammation with thrombosis. Inflammasome activation and subsequent pyroptosis are critical defense mechanisms against microbes. However, overactivation of inflammasome leads to death of the host. Although recent studies have uncovered the mechanism of pyroptosis following inflammasome activation, how pyroptotic cell death drives pathogenesis, eventually leading to death of the host, is unknown. Here, we identified inflammasome activation as a trigger for blood clotting through pyroptosis. We have shown that canonical inflammasome activation by the conserved type III secretion system (T3SS) rod proteins from Gram-negative bacteria or noncanonical inflammasome activation by lipopolysaccharide (LPS) induced systemic blood clotting and massive thrombosis in tissues. Following inflammasome activation, pyroptotic macrophages released tissue factor (TF), an essential initiator of coagulation cascades. Genetic or pharmacological inhibition of TF abolishes inflammasome-mediated blood clotting and protects against death. Our data reveal that blood clotting is the major cause of host death following inflammasome activation and demonstrate that inflammasome bridges inflammation with thrombosis. [Display omitted] •Canonical or noncanonical inflammasome activation leads to blood clotting•Inflammasome activation induces blood clotting through pyroptosis•Tissue factor released from pyroptotic macrophages drives blood blotting•Interfering tissue factor prevents pyroptosis-induced lethality Overactivation of inflammasome leads to death of the host. Wu and colleagues demonstrate that activation of coagulation is responsible for inflammasome activation-induced death. Inflammasome activation and subsequent pyroptosis are critical defense mechanisms against microbes. However, overactivation of inflammasome leads to death of the host. Although recent studies have uncovered the mechanism of pyroptosis following inflammasome activation, how pyroptotic cell death drives pathogenesis, eventually leading to death of the host, is unknown. Here, we identified inflammasome activation as a trigger for blood clotting through pyroptosis. We have shown that canonical inflammasome activation by the conserved type III secretion system (T3SS) rod proteins from Gram-negative bacteria or noncanonical inflammasome activation by lipopolysaccharide (LPS) induced systemic blood clotting and massive thrombosis in tissues. Following inflammasome activation, pyroptotic macrophages released tissue factor (TF), an essential initiator of coagulation cascades. Genetic or pharmacological inhibition of TF abolishes inflammasome-mediated blood clotting and protects against death. Our data reveal that blood clotting is the major cause of host death following inflammasome activation and demonstrate that inflammasome bridges inflammation with thrombosis.Inflammasome activation and subsequent pyroptosis are critical defense mechanisms against microbes. However, overactivation of inflammasome leads to death of the host. Although recent studies have uncovered the mechanism of pyroptosis following inflammasome activation, how pyroptotic cell death drives pathogenesis, eventually leading to death of the host, is unknown. Here, we identified inflammasome activation as a trigger for blood clotting through pyroptosis. We have shown that canonical inflammasome activation by the conserved type III secretion system (T3SS) rod proteins from Gram-negative bacteria or noncanonical inflammasome activation by lipopolysaccharide (LPS) induced systemic blood clotting and massive thrombosis in tissues. Following inflammasome activation, pyroptotic macrophages released tissue factor (TF), an essential initiator of coagulation cascades. Genetic or pharmacological inhibition of TF abolishes inflammasome-mediated blood clotting and protects against death. Our data reveal that blood clotting is the major cause of host death following inflammasome activation and demonstrate that inflammasome bridges inflammation with thrombosis. Inflammasome activation and subsequent pyroptosis are critical defense mechanisms against microbes. However, overactivation of inflammasome leads to death of the host. While recent studies have uncovered the mechanism of pyroptosis following inflammasome activation, how pyroptotic cell death drives pathogenesis eventually leading to death of the host is unknown. Here we identified inflammasome activation as a trigger for blood clotting through pyroptosis. We have shown that canonical inflammasome activation by the conserved type III secretion system (T3SS) rod proteins from Gram-negative bacteria or noncanonical inflammasome activation by lipopolysaccharide (LPS) induced systemic blood clotting and massive thrombosis in tissues. Following inflammasome activation, pyroptotic macrophages released tissue factor (TF), an essential initiator of coagulation cascades. Genetic or pharmacological inhibition of TF abolished inflammasome-mediated blood clotting and protects against death. Our data reveal that blood clotting is the major cause of host death following inflammasome activation and demonstrate that inflammasome bridges inflammation with thrombosis. Overactivation of inflammasome leads to death of the host. Wu and colleagues demonstrate that activation of coagulation is responsible for inflammasome activation-induced death. Inflammasome activation and subsequent pyroptosis are critical defense mechanisms against microbes. However, overactivation of inflammasome leads to death of the host. Although recent studies have uncovered the mechanism of pyroptosis following inflammasome activation, how pyroptotic cell death drives pathogenesis, eventually leading to death of the host, is unknown. Here, we identified inflammasome activation as a trigger for blood clotting through pyroptosis. We have shown that canonical inflammasome activation by the conserved type III secretion system (T3SS) rod proteins from Gram-negative bacteria or noncanonical inflammasome activation by lipopolysaccharide (LPS) induced systemic blood clotting and massive thrombosis in tissues. Following inflammasome activation, pyroptotic macrophages released tissue factor (TF), an essential initiator of coagulation cascades. Genetic or pharmacological inhibition of TF abolishes inflammasome-mediated blood clotting and protects against death. Our data reveal that blood clotting is the major cause of host death following inflammasome activation and demonstrate that inflammasome bridges inflammation with thrombosis. |
| Author | Wu, Congqing Lu, Wei Mackman, Nigel Zhang, Xinyi Wei, Yinan Li, Lan Xiang, Binggang Hisada, Yohei Daugherty, Alan Shi, Jumei Smyth, Susan S. Kirchhofer, Daniel Li, Xiang-An Li, Zhenyu Grover, Steven P. Shao, Feng Shi, Xuyan Zhang, Guoying Zhang, Yan Shiroishi, Toshihiko |
| AuthorAffiliation | 4 Department of Medicine, Division of Hematology and Oncology, McAllister Heart Institute, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA 9 Mammalian Genetics Laboratory, Genetic Strains Research Center, National Institute of Genetics, Mishima, Shizuoka, Japan 8 Department of Early Discovery Biochemistry, Genentech, Inc., South San Francisco, CA, USA 1 Saha Cardiovascular Research Center, College of Medicine, University of Kentucky, Lexington, KY, USA 3 National Institute of Biological Sciences, Beijing, China 7 Veterans Affairs Medical Center, Lexington, KY, USA 2 Department of Chemistry, College of Arts and Sciences, University of Kentucky, Lexington, KY, USA 5 Department of Hematology, Shanghai Tenth People’s Hospital, Tongji University Cancer Center, Tongji University School of Medicine, Shanghai, China 6 Department of Physiology, College of Medicine, University of Kentucky, Lexington, KY, USA |
| AuthorAffiliation_xml | – name: 4 Department of Medicine, Division of Hematology and Oncology, McAllister Heart Institute, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA – name: 6 Department of Physiology, College of Medicine, University of Kentucky, Lexington, KY, USA – name: 5 Department of Hematology, Shanghai Tenth People’s Hospital, Tongji University Cancer Center, Tongji University School of Medicine, Shanghai, China – name: 3 National Institute of Biological Sciences, Beijing, China – name: 7 Veterans Affairs Medical Center, Lexington, KY, USA – name: 8 Department of Early Discovery Biochemistry, Genentech, Inc., South San Francisco, CA, USA – name: 9 Mammalian Genetics Laboratory, Genetic Strains Research Center, National Institute of Genetics, Mishima, Shizuoka, Japan – name: 2 Department of Chemistry, College of Arts and Sciences, University of Kentucky, Lexington, KY, USA – name: 1 Saha Cardiovascular Research Center, College of Medicine, University of Kentucky, Lexington, KY, USA |
| Author_xml | – sequence: 1 givenname: Congqing surname: Wu fullname: Wu, Congqing organization: Saha Cardiovascular Research Center, College of Medicine, University of Kentucky, Lexington, KY, USA – sequence: 2 givenname: Wei surname: Lu fullname: Lu, Wei organization: Department of Chemistry, College of Arts and Sciences, University of Kentucky, Lexington, KY, USA – sequence: 3 givenname: Yan surname: Zhang fullname: Zhang, Yan organization: Saha Cardiovascular Research Center, College of Medicine, University of Kentucky, Lexington, KY, USA – sequence: 4 givenname: Guoying surname: Zhang fullname: Zhang, Guoying organization: Saha Cardiovascular Research Center, College of Medicine, University of Kentucky, Lexington, KY, USA – sequence: 5 givenname: Xuyan surname: Shi fullname: Shi, Xuyan organization: National Institute of Biological Sciences, Beijing, China – sequence: 6 givenname: Yohei surname: Hisada fullname: Hisada, Yohei organization: Division of Hematology and Oncology, Department of Medicine, McAllister Heart Institute, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA – sequence: 7 givenname: Steven P. surname: Grover fullname: Grover, Steven P. organization: Division of Hematology and Oncology, Department of Medicine, McAllister Heart Institute, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA – sequence: 8 givenname: Xinyi surname: Zhang fullname: Zhang, Xinyi organization: Department of Chemistry, College of Arts and Sciences, University of Kentucky, Lexington, KY, USA – sequence: 9 givenname: Lan surname: Li fullname: Li, Lan organization: Department of Chemistry, College of Arts and Sciences, University of Kentucky, Lexington, KY, USA – sequence: 10 givenname: Binggang surname: Xiang fullname: Xiang, Binggang organization: Saha Cardiovascular Research Center, College of Medicine, University of Kentucky, Lexington, KY, USA – sequence: 11 givenname: Jumei surname: Shi fullname: Shi, Jumei organization: Department of Hematology, Shanghai Tenth People’s Hospital, Tongji University Cancer Center, Tongji University School of Medicine, Shanghai, China – sequence: 12 givenname: Xiang-An surname: Li fullname: Li, Xiang-An organization: Department of Physiology, College of Medicine, University of Kentucky, Lexington, KY, USA – sequence: 13 givenname: Alan surname: Daugherty fullname: Daugherty, Alan organization: Saha Cardiovascular Research Center, College of Medicine, University of Kentucky, Lexington, KY, USA – sequence: 14 givenname: Susan S. surname: Smyth fullname: Smyth, Susan S. organization: Saha Cardiovascular Research Center, College of Medicine, University of Kentucky, Lexington, KY, USA – sequence: 15 givenname: Daniel surname: Kirchhofer fullname: Kirchhofer, Daniel organization: Department of Early Discovery Biochemistry, Genentech, Inc., South San Francisco, CA, USA – sequence: 16 givenname: Toshihiko surname: Shiroishi fullname: Shiroishi, Toshihiko organization: Mammalian Genetics Laboratory, Genetic Strains Research Center, National Institute of Genetics, Mishima, Shizuoka, Japan – sequence: 17 givenname: Feng surname: Shao fullname: Shao, Feng organization: National Institute of Biological Sciences, Beijing, China – sequence: 18 givenname: Nigel surname: Mackman fullname: Mackman, Nigel organization: Division of Hematology and Oncology, Department of Medicine, McAllister Heart Institute, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA – sequence: 19 givenname: Yinan surname: Wei fullname: Wei, Yinan email: yinan.wei@uky.edu organization: Department of Chemistry, College of Arts and Sciences, University of Kentucky, Lexington, KY, USA – sequence: 20 givenname: Zhenyu surname: Li fullname: Li, Zhenyu email: zhenyuli08@uky.edu organization: Saha Cardiovascular Research Center, College of Medicine, University of Kentucky, Lexington, KY, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31076358$$D View this record in MEDLINE/PubMed |
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| Keywords | GSDMD pyroptosis tissue factor inflammasome macrophage coagulation LPS sepsis caspase DIC |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 AUTHOR CONTRIBUTIONS Lead contact: zhenyuli08@uky.edu (Z.L.) C.W., Y.W. and Z.L. designed and performed the experiments and wrote the manuscript, assisted by W.L., Y.Z., G.Z., X.S., Y.H., S.P.G., X.Z., L.L., B.X., and J.S. X.L., A.D., S.S.S., N.M. and F.S. contributed to manuscript preparation. D.K., T.S., and N.M. provided mice and/or reagents and discussed experiments. All authors discussed the results and commented on the manuscript. |
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| Snippet | Inflammasome activation and subsequent pyroptosis are critical defense mechanisms against microbes. However, overactivation of inflammasome leads to death of... SummaryInflammasome activation and subsequent pyroptosis are critical defense mechanisms against microbes. However, overactivation of inflammasome leads to... |
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| SubjectTerms | Animals Apoptosis Bacterial infections Bacterial Infections - complications Bacterial Infections - microbiology Biomarkers Blood Blood Coagulation Cascades caspase Caspases - metabolism Cell activation Cell culture Cell death Cell-Derived Microparticles - immunology Cell-Derived Microparticles - metabolism Cloning Clotting Coagulation Cytotoxicity DIC Disease Models, Animal E coli Gram-negative bacteria GSDMD Humans inflammasome Inflammasomes Inflammasomes - metabolism Lipopolysaccharides Lipopolysaccharides - immunology LPS macrophage Macrophages Macrophages - immunology Macrophages - metabolism Mice Microscopy Monocytes - immunology Monocytes - metabolism Mortality Pathogenesis Pharmacology Proteins Pyroptosis Secretion Sepsis Signal Transduction Thromboembolism Thromboplastin - metabolism Thrombosis Thrombosis - blood Thrombosis - etiology Thrombosis - metabolism Thrombosis - mortality Time series Tissue factor |
| Title | Inflammasome Activation Triggers Blood Clotting and Host Death through Pyroptosis |
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