Mechanosensation of cyclical force by PIEZO1 is essential for innate immunity
Direct recognition of invading pathogens by innate immune cells is a critical driver of the inflammatory response. However, cells of the innate immune system can also sense their local microenvironment and respond to physiological fluctuations in temperature, pH, oxygen and nutrient availability, wh...
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| Published in | Nature (London) Vol. 573; no. 7772; pp. 69 - 74 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
01.09.2019
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0028-0836 1476-4687 1476-4687 |
| DOI | 10.1038/s41586-019-1485-8 |
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| Abstract | Direct recognition of invading pathogens by innate immune cells is a critical driver of the inflammatory response. However, cells of the innate immune system can also sense their local microenvironment and respond to physiological fluctuations in temperature, pH, oxygen and nutrient availability, which are altered during inflammation. Although cells of the immune system experience force and pressure throughout their life cycle, little is known about how these mechanical processes regulate the immune response. Here we show that cyclical hydrostatic pressure, similar to that experienced by immune cells in the lung, initiates an inflammatory response via the mechanically activated ion channel PIEZO1. Mice lacking PIEZO1 in innate immune cells showed ablated pulmonary inflammation in the context of bacterial infection or fibrotic autoinflammation. Our results reveal an environmental sensory axis that stimulates innate immune cells to mount an inflammatory response, and demonstrate a physiological role for PIEZO1 and mechanosensation in immunity.
PIEZO1 signalling mediates activation of a proinflammatory response to cyclical pressure fluctuations in immune cells. |
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| AbstractList | Direct recognition of invading pathogens by innate immune cells is a critical driver of the inflammatory response. However, cells of the innate immune system can also sense their local microenvironment and respond to physiological fluctuations in temperature, pH, oxygen and nutrient availability, which are altered during inflammation. Although cells of the immune system experience force and pressure throughout their life cycle, little is known about how these mechanical processes regulate the immune response. Here we show that cyclical hydrostatic pressure, similar to that experienced by immune cells in the lung, initiates an inflammatory response via the mechanically activated ion channel PIEZO1. Mice lacking PIEZO1 in innate immune cells showed ablated pulmonary inflammation in the context of bacterial infection or fibrotic autoinflammation. Our results reveal an environmental sensory axis that stimulates innate immune cells to mount an inflammatory response, and demonstrate a physiological role for PIEZO1 and mechanosensation in immunity. Direct recognition of invading pathogens by innate immune cells is a critical driver of the inflammatory response. However, cells of the innate immune system can also sense their local microenvironment and respond to physiological fluctuations in temperature, pH, oxygen and nutrient availability, which are altered during inflammation. Although cells of the immune system experience force and pressure throughout their life cycle, little is known about how these mechanical processes regulate the immune response. Here we show that cyclical hydrostatic pressure, similar to that experienced by immune cells in the lung, initiates an inflammatory response via the mechanically activated ion channel PIEZO1. Mice lacking PIEZO1 in innate immune cells showed ablated pulmonary inflammation in the context of bacterial infection or fibrotic autoinflammation. Our results reveal an environmental sensory axis that stimulates innate immune cells to mount an inflammatory response, and demonstrate a physiological role for PIEZO1 and mechanosensation in immunity. PIEZO1 signalling mediates activation of a proinflammatory response to cyclical pressure fluctuations in immune cells. Although cells of the immune system experience force and pressure throughout their lifecycle, almost nothing is known about how these mechanical processes regulate the immune response 1 . Both tissue-resident and tissue-infiltrating immune cells in highly mechanical organs, such as the lung, are constantly exposed to tonic and dynamically changing mechanical cues 2 . Here using reverse genetics, we show that myeloid cells respond to force and alterations in cyclical hydrostatic pressure via the mechanosensory ion channel PIEZO1 3 . Unbiased RNA sequencing from macrophages subjected to cyclical hydrostatic pressure reveals a striking state of proinflammatory reprogramming. We report a novel mechanosensory-immune signaling circuit which PIEZO1 initiates in response to cyclical hydrostatic pressure, driving c-JUN activation and transcriptional upregulation of Endothelin-1 (EDN1). EDN1 in turn stabilizes HIF1α, which facilitates transcription of a potent and prolonged program of proinflammatory mediators. Using mice conditionally deficient of PIEZO1 in myeloid cells, and cellular depletion assays, we show infiltrating monocytes respond to cyclical force to recruit neutrophils and clear pulmonary Pseudomonas aeruginosa infection via EDN1. Furthermore, myeloid PIEZO1 also drove lung pathology in a mouse model of pulmonary fibrosis. Our results demonstrate a novel environmental sensory axis that myeloid cells recognize to mount an inflammatory response and is the first report showing a physiological role for PIEZO1 and mechanosensation in immunity. Direct recognition of invading pathogens by innate immune cells is a critical driver of the inflammatory response. However, cells of the innate immune system can also sense their local microenvironment and respond to physiological fluctuations in temperature, pH, oxygen and nutrient availability, which are altered during inflammation. Although cells of the immune system experience force and pressure throughout their life cycle, little is known about how these mechanical processes regulate the immune response. Here we show that cyclical hydrostatic pressure, similar to that experienced by immune cells in the lung, initiates an inflammatory response via the mechanically activated ion channel PIEZO1. Mice lacking PIEZO1 in innate immune cells showed ablated pulmonary inflammation in the context of bacterial infection or fibrotic autoinflammation. Our results reveal an environmental sensory axis that stimulates innate immune cells to mount an inflammatory response, and demonstrate a physiological role for PIEZO1 and mechanosensation in immunity. PIEZO1 signalling mediates activation of a proinflammatory response to cyclical pressure fluctuations in immune cells. Direct recognition of invading pathogens by innate immune cells is a critical driver of the inflammatory response. However, cells of the innate immune system can also sense their local microenvironment and respond to physiological fluctuations in temperature, pH, oxygen and nutrient availability, which are altered during inflammation. Although cells of the immune system experience force and pressure throughout their life cycle, little is known about how these mechanical processes regulate the immune response. Here we show that cyclical hydrostatic pressure, similar to that experienced by immune cells in the lung, initiates an inflammatory response via the mechanically activated ion channel PIEZO1. Mice lacking PIEZO1 in innate immune cells showed ablated pulmonary inflammation in the context of bacterial infection or fibrotic autoinflammation. Our results reveal an environmental sensory axis that stimulates innate immune cells to mount an inflammatory response, and demonstrate a physiological role for PIEZO1 and mechanosensation in immunity.Direct recognition of invading pathogens by innate immune cells is a critical driver of the inflammatory response. However, cells of the innate immune system can also sense their local microenvironment and respond to physiological fluctuations in temperature, pH, oxygen and nutrient availability, which are altered during inflammation. Although cells of the immune system experience force and pressure throughout their life cycle, little is known about how these mechanical processes regulate the immune response. Here we show that cyclical hydrostatic pressure, similar to that experienced by immune cells in the lung, initiates an inflammatory response via the mechanically activated ion channel PIEZO1. Mice lacking PIEZO1 in innate immune cells showed ablated pulmonary inflammation in the context of bacterial infection or fibrotic autoinflammation. Our results reveal an environmental sensory axis that stimulates innate immune cells to mount an inflammatory response, and demonstrate a physiological role for PIEZO1 and mechanosensation in immunity. |
| Audience | Academic |
| Author | Harman, Christian C. D. Yun, Sanguk Steach, Holly R. Flavell, Richard A. Jackson, Ruaidhrí Palm, Noah W. Dela Cruz, Charles. S. Solis, Angel G. de Zoete, Marcel R. To, S. D. Filip York, Autumn G. Schwartz, Martin A. Sharma, Lokesh Mack, Matthias Warnock, James N. Bielecki, Piotr |
| AuthorAffiliation | 7 Department of Agricultural and Biological Engineering, Mississippi State University, Mississippi State, MS 39759, USA 5 Department of Infectious Diseases and Immunology, Utrecht University, Utrecht, Netherlands 4 Department of Internal Medicine, Yale Cardiovascular Research Center, Yale University, New Haven, CT 06520, USA 8 Department of Internal Medicine II – Nephrology, University Hospital Regensburg 93042 Regensburg, Germany 1 Department of Immunobiology, Yale University School of Medicine, New Haven, CT 06520, USA 6 School of Chemical, Materials and Biomedical Engineering, University of Georgia, Athens GA, 30602, USA 9 Howard Hughes Medical Institute, Yale University, New Haven, CT 06520, USA 2 Department of Internal Medicine, Pulmonary, Critical Care and Sleep Medicine, Yale School of Medicine, New Haven, CT 06520, USA 3 Department of Genetics, Yale University School of Medicine, New Haven, CT 06520, USA |
| AuthorAffiliation_xml | – name: 3 Department of Genetics, Yale University School of Medicine, New Haven, CT 06520, USA – name: 6 School of Chemical, Materials and Biomedical Engineering, University of Georgia, Athens GA, 30602, USA – name: 9 Howard Hughes Medical Institute, Yale University, New Haven, CT 06520, USA – name: 5 Department of Infectious Diseases and Immunology, Utrecht University, Utrecht, Netherlands – name: 7 Department of Agricultural and Biological Engineering, Mississippi State University, Mississippi State, MS 39759, USA – name: 8 Department of Internal Medicine II – Nephrology, University Hospital Regensburg 93042 Regensburg, Germany – name: 1 Department of Immunobiology, Yale University School of Medicine, New Haven, CT 06520, USA – name: 2 Department of Internal Medicine, Pulmonary, Critical Care and Sleep Medicine, Yale School of Medicine, New Haven, CT 06520, USA – name: 4 Department of Internal Medicine, Yale Cardiovascular Research Center, Yale University, New Haven, CT 06520, USA |
| Author_xml | – sequence: 1 givenname: Angel G. surname: Solis fullname: Solis, Angel G. organization: Department of Immunobiology, Yale University School of Medicine – sequence: 2 givenname: Piotr surname: Bielecki fullname: Bielecki, Piotr organization: Department of Immunobiology, Yale University School of Medicine – sequence: 3 givenname: Holly R. surname: Steach fullname: Steach, Holly R. organization: Department of Immunobiology, Yale University School of Medicine – sequence: 4 givenname: Lokesh surname: Sharma fullname: Sharma, Lokesh organization: Department of Internal Medicine, Pulmonary, Critical Care and Sleep Medicine, Yale School of Medicine – sequence: 5 givenname: Christian C. D. surname: Harman fullname: Harman, Christian C. D. organization: Department of Genetics, Yale University School of Medicine – sequence: 6 givenname: Sanguk surname: Yun fullname: Yun, Sanguk organization: Department of Internal Medicine (Cardiology), Yale Cardiovascular Research Center, Yale University, Department of Cell Biology, Yale Cardiovascular Research Center, Yale University, Department of Biomedical Engineering, Yale Cardiovascular Research Center, Yale University, Yale University – sequence: 7 givenname: Marcel R. surname: de Zoete fullname: de Zoete, Marcel R. organization: Department of Infectious Diseases and Immunology, Utrecht University – sequence: 8 givenname: James N. surname: Warnock fullname: Warnock, James N. organization: School of Chemical, Materials and Biomedical Engineering, University of Georgia – sequence: 9 givenname: S. D. Filip surname: To fullname: To, S. D. Filip organization: Department of Agricultural and Biological Engineering, Mississippi State University – sequence: 10 givenname: Autumn G. surname: York fullname: York, Autumn G. organization: Department of Immunobiology, Yale University School of Medicine – sequence: 11 givenname: Matthias surname: Mack fullname: Mack, Matthias organization: Department of Internal Medicine II—Nephrology, University Hospital Regensburg – sequence: 12 givenname: Martin A. surname: Schwartz fullname: Schwartz, Martin A. organization: Department of Internal Medicine (Cardiology), Yale Cardiovascular Research Center, Yale University, Department of Cell Biology, Yale Cardiovascular Research Center, Yale University, Department of Biomedical Engineering, Yale Cardiovascular Research Center, Yale University, Yale University – sequence: 13 givenname: Charles. S. surname: Dela Cruz fullname: Dela Cruz, Charles. S. organization: Department of Internal Medicine, Pulmonary, Critical Care and Sleep Medicine, Yale School of Medicine – sequence: 14 givenname: Noah W. surname: Palm fullname: Palm, Noah W. organization: Department of Immunobiology, Yale University School of Medicine – sequence: 15 givenname: Ruaidhrí surname: Jackson fullname: Jackson, Ruaidhrí email: ruaidhri.jackson@yale.edu organization: Department of Immunobiology, Yale University School of Medicine – sequence: 16 givenname: Richard A. surname: Flavell fullname: Flavell, Richard A. email: richard.flavell@yale.edu organization: Department of Immunobiology, Yale University School of Medicine, Howard Hughes Medical Institute, Yale University |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31435009$$D View this record in MEDLINE/PubMed |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 A.G.S. designed and performed experiments, collected and analyzed data, and wrote the manuscript. P.B. performed microbiological experiments and offered vital conceptual insight. H.R.S. developed reagents and performed Cas9 experiments. L.S. performed in vivo fibrosis experiments. C.C.D.H performed all bioinformatical analysis. S.Y. performed in vitro shear stress experiments. N.W.P. and M.R.D.Z generated mice and offered conceptual insight. J.N.W. and S.D.F.T. designed and built the bioreactor and software necessary to complete mechanistic experiments. A.G.Y. helped collect samples. M.M. provided critical reagents and advice on experimental design. M.A.S. and C.S.D.C. provided intellectual support. R.J. and R.A.F supervised the project, helped interpret the work, and supervised writing of the manuscript. Contributions |
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| Snippet | Direct recognition of invading pathogens by innate immune cells is a critical driver of the inflammatory response. However, cells of the innate immune system... Although cells of the immune system experience force and pressure throughout their lifecycle, almost nothing is known about how these mechanical processes... |
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| SubjectTerms | 13/21 13/31 14/1 14/63 38/39 38/90 38/91 42/109 42/41 42/44 631/250/262 631/250/516 Ablation Animals Bacterial diseases Bacterial infections Endothelin-1 - metabolism Female Fibrosis Gene expression Humanities and Social Sciences Hydrostatic Pressure Hypoxia Hypoxia-Inducible Factor 1, alpha Subunit - metabolism Immune response Immune system Immunity Immunity, Innate Infections Inflammation Inflammation - immunology Inflammation - metabolism Inflammation - microbiology Inflammatory response Innate immunity Ion channels Ion Channels - metabolism JNK Mitogen-Activated Protein Kinases - metabolism Kinases Life cycles Lung - immunology Lung - metabolism Lung - microbiology Lungs Macrophages - immunology Macrophages - metabolism Male Mechanical properties Mechanotransduction Mechanotransduction, Cellular - immunology Mice Motility multidisciplinary Nutrient availability Oxygen Physiological aspects Physiology Pressure Pseudomonas aeruginosa - immunology Pseudomonas Infections - immunology Pulmonary arteries Pulmonary fibrosis Science Science (multidisciplinary) Signal Transduction Variation |
| Title | Mechanosensation of cyclical force by PIEZO1 is essential for innate immunity |
| URI | https://link.springer.com/article/10.1038/s41586-019-1485-8 https://www.ncbi.nlm.nih.gov/pubmed/31435009 https://www.proquest.com/docview/2290912008 https://www.proquest.com/docview/2284557405 https://pubmed.ncbi.nlm.nih.gov/PMC6939392 |
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