Detection of a microbial metabolite by STING regulates inflammasome activation in response to Chlamydia trachomatis infection
The innate immune system is a critical component of host defence against microbial pathogens, but effective responses require an ability to distinguish between infectious and non-infectious insult to prevent inappropriate inflammation. Using the important obligate intracellular human pathogen Chlamy...
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| Published in | PLoS pathogens Vol. 13; no. 6; p. e1006383 |
|---|---|
| Main Authors | , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
01.06.2017
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
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| Abstract | The innate immune system is a critical component of host defence against microbial pathogens, but effective responses require an ability to distinguish between infectious and non-infectious insult to prevent inappropriate inflammation. Using the important obligate intracellular human pathogen Chlamydia trachomatis; an organism that causes significant immunopathology, we sought to determine critical host and pathogen factors that contribute to the induction of inflammasome activation. We assayed inflammasome activation by immunoblotting and ELISA to detect IL-1β processing and LDH release to determine pyroptosis. Using primary murine bone marrow derived macrophages or human monocyte derived dendritic cells, infected with live or attenuated Chlamydia trachomatis we report that the live organism activates both canonical and non-canonical inflammasomes, but only canonical inflammasomes controlled IL-1β processing which preceded pyroptosis. NADPH oxidase deficient macrophages were permissive to Chlamydia trachomatis replication and displayed elevated type-1 interferon and inflammasome activation. Conversely, attenuated, non-replicating Chlamydia trachomatis, primed but did not activate inflammasomes and stimulated reduced type-1 interferon responses. This suggested bacterial replication or metabolism as important factors that determine interferon responses and inflammasome activation. We identified STING but not cGAS as a central mediator of interferon regulated inflammasome activation. Interestingly, exogenous delivery of a Chlamydia trachomatis metabolite and STING ligand-cyclic di-AMP, recovered inflammasome activation to attenuated bacteria in a STING dependent manner thus indicating that a bacterial metabolite is a key factor initiating inflammasome activation through STING, independent of cGAS. These data suggest a potential mechanism of how the innate immune system can distinguish between infectious and non-infectious insult and instigate appropriate immune responses that could be therapeutically targeted. |
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| AbstractList | The innate immune system is a critical component of host defence against microbial pathogens, but effective responses require an ability to distinguish between infectious and non-infectious insult to prevent inappropriate inflammation. Using the important obligate intracellular human pathogen Chlamydia trachomatis; an organism that causes significant immunopathology, we sought to determine critical host and pathogen factors that contribute to the induction of inflammasome activation. We assayed inflammasome activation by immunoblotting and ELISA to detect IL-1β processing and LDH release to determine pyroptosis. Using primary murine bone marrow derived macrophages or human monocyte derived dendritic cells, infected with live or attenuated Chlamydia trachomatis we report that the live organism activates both canonical and non-canonical inflammasomes, but only canonical inflammasomes controlled IL-1β processing which preceded pyroptosis. NADPH oxidase deficient macrophages were permissive to Chlamydia trachomatis replication and displayed elevated type-1 interferon and inflammasome activation. Conversely, attenuated, non-replicating Chlamydia trachomatis, primed but did not activate inflammasomes and stimulated reduced type-1 interferon responses. This suggested bacterial replication or metabolism as important factors that determine interferon responses and inflammasome activation. We identified STING but not cGAS as a central mediator of interferon regulated inflammasome activation. Interestingly, exogenous delivery of a Chlamydia trachomatis metabolite and STING ligand-cyclic di-AMP, recovered inflammasome activation to attenuated bacteria in a STING dependent manner thus indicating that a bacterial metabolite is a key factor initiating inflammasome activation through STING, independent of cGAS. These data suggest a potential mechanism of how the innate immune system can distinguish between infectious and non-infectious insult and instigate appropriate immune responses that could be therapeutically targeted. The innate immune system is a critical component of host defence against microbial pathogens, but effective responses require an ability to distinguish between infectious and noninfectious insult to prevent inappropriate inflammation. Using the important obligate intracellular human pathogen Chlamydia trachomatis; an organism that causes significant immunopathology, we sought to determine critical host and pathogen factors that contribute to the induction of inflammasome activation. We assayed inflammasome activation by immunoblotting and ELISA to detect IL-1 beta processing and LDH release to determine pyroptosis. Using primary murine bone marrow derived macrophages or human monocyte derived dendritic cells, infected with live or attenuated Chlamydia trachomatis we report that the live organism activates both canonical and non-canonical inflammasomes, but only canonical inflammasomes controlled IL-1 beta processing which preceded pyroptosis. NADPH oxidase deficient macrophages were permissive to Chlamydia trachomatis replication and displayed elevated type-1 interferon and inflammasome activation. Conversely, attenuated, non-replicating Chlamydia trachomatis, primed but did not activate inflammasomes and stimulated reduced type-1 interferon responses. This suggested bacterial replication or metabolism as important factors that determine interferon responses and inflammasome activation. We identified STING but not cGAS as a central mediator of interferon regulated inflammasome activation. Interestingly, exogenous delivery of a Chlamydia trachomatis metabolite and STING ligand D cyclic di-AMP, recovered inflammasome activation to attenuated bacteria in a STING dependent manner thus indicating that a bacterial metabolite is a key factor initiating inflammasome activation through STING, independent of cGAS. These data suggest a potential mechanism of how the innate immune system can distinguish between infectious and non-infectious insult and instigate appropriate immune responses that could be therapeutically targeted. The innate immune system is a critical component of host defence against microbial pathogens, but effective responses require an ability to distinguish between infectious and non-infectious insult to prevent inappropriate inflammation. Using the important obligate intracellular human pathogen Chlamydia trachomatis; an organism that causes significant immunopathology, we sought to determine critical host and pathogen factors that contribute to the induction of inflammasome activation. We assayed inflammasome activation by immunoblotting and ELISA to detect IL-1β processing and LDH release to determine pyroptosis. Using primary murine bone marrow derived macrophages or human monocyte derived dendritic cells, infected with live or attenuated Chlamydia trachomatis we report that the live organism activates both canonical and non-canonical inflammasomes, but only canonical inflammasomes controlled IL-1β processing which preceded pyroptosis. NADPH oxidase deficient macrophages were permissive to Chlamydia trachomatis replication and displayed elevated type-1 interferon and inflammasome activation. Conversely, attenuated, non-replicating Chlamydia trachomatis , primed but did not activate inflammasomes and stimulated reduced type-1 interferon responses. This suggested bacterial replication or metabolism as important factors that determine interferon responses and inflammasome activation. We identified STING but not cGAS as a central mediator of interferon regulated inflammasome activation. Interestingly, exogenous delivery of a Chlamydia trachomatis metabolite and STING ligand—cyclic di-AMP, recovered inflammasome activation to attenuated bacteria in a STING dependent manner thus indicating that a bacterial metabolite is a key factor initiating inflammasome activation through STING, independent of cGAS. These data suggest a potential mechanism of how the innate immune system can distinguish between infectious and non-infectious insult and instigate appropriate immune responses that could be therapeutically targeted. Innate responses to bacterial infection such as Chlamydia trachomatis activate inflammasomes to enable the processing of IL-1β, IL-18 and the induction of an inflammatory form of cell death termed pyroptosis. Inflammasomes are crucial to host defence but require tight regulation in order to prevent inappropriate inflammation and immunopathology. Here, we demonstrate that the pro-inflammatory potential of an attenuated strain of Chlamydia trachomatis , that fails to activate the inflammasome, can be rescued by the addition of a bacterial metabolite. The requirement for this metabolite, highlights a novel mechanism of inflammasome regulation and reveals a crucial role for STING mediated interferon signalling independent of cGAS. These findings further our understanding of how the innate immune system can differentiate between potential infectious and non-infectious threats and mount appropriate immune responses. The innate immune system is a critical component of host defence against microbial pathogens, but effective responses require an ability to distinguish between infectious and non-infectious insult to prevent inappropriate inflammation. Using the important obligate intracellular human pathogen Chlamydia trachomatis; an organism that causes significant immunopathology, we sought to determine critical host and pathogen factors that contribute to the induction of inflammasome activation. We assayed inflammasome activation by immunoblotting and ELISA to detect IL-1[Beta] processing and LDH release to determine pyroptosis. Using primary murine bone marrow derived macrophages or human monocyte derived dendritic cells, infected with live or attenuated Chlamydia trachomatis we report that the live organism activates both canonical and non-canonical inflammasomes, but only canonical inflammasomes controlled IL-1[Beta] processing which preceded pyroptosis. NADPH oxidase deficient macrophages were permissive to Chlamydia trachomatis replication and displayed elevated type-1 interferon and inflammasome activation. Conversely, attenuated, non-replicating Chlamydia trachomatis, primed but did not activate inflammasomes and stimulated reduced type-1 interferon responses. This suggested bacterial replication or metabolism as important factors that determine interferon responses and inflammasome activation. We identified STING but not cGAS as a central mediator of interferon regulated inflammasome activation. Interestingly, exogenous delivery of a Chlamydia trachomatis metabolite and STING ligand-cyclic di-AMP, recovered inflammasome activation to attenuated bacteria in a STING dependent manner thus indicating that a bacterial metabolite is a key factor initiating inflammasome activation through STING, independent of cGAS. These data suggest a potential mechanism of how the innate immune system can distinguish between infectious and non-infectious insult and instigate appropriate immune responses that could be therapeutically targeted. |
| Audience | Academic |
| Author | Gekara, Nelson O Brode, Sven Elder, Matthew J Bryant, Clare Tourlomousis, Panagiotis Fitzmaurice, Timothy J Clare, Simon Chee, Ronnie Webster, Steve J Gaston, Hill J S Goodall, Jane C Ellis, Lou |
| AuthorAffiliation | 1 Rheumatology Research Group, Department of Medicine, University of Cambridge, Cambridge, United Kingdom 2 Molecular Infection Medicine Sweden, Umeå Centre for Microbial Research, Department of Molecular Biology, Umeå University, Umeå, Sweden 4 Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, United Kingdom University of São Paulo FMRP/USP, BRAZIL 3 Department of Veterinary Medicine, University of Cambridge, Cambridge, United Kingdom 5 Department of Immunology, Royal Free Hospital, London, United Kingdom |
| AuthorAffiliation_xml | – name: 4 Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, United Kingdom – name: University of São Paulo FMRP/USP, BRAZIL – name: 5 Department of Immunology, Royal Free Hospital, London, United Kingdom – name: 2 Molecular Infection Medicine Sweden, Umeå Centre for Microbial Research, Department of Molecular Biology, Umeå University, Umeå, Sweden – name: 1 Rheumatology Research Group, Department of Medicine, University of Cambridge, Cambridge, United Kingdom – name: 3 Department of Veterinary Medicine, University of Cambridge, Cambridge, United Kingdom |
| Author_xml | – sequence: 1 givenname: Steve J orcidid: 0000-0002-0864-1182 surname: Webster fullname: Webster, Steve J organization: Rheumatology Research Group, Department of Medicine, University of Cambridge, Cambridge, United Kingdom – sequence: 2 givenname: Sven surname: Brode fullname: Brode, Sven organization: Rheumatology Research Group, Department of Medicine, University of Cambridge, Cambridge, United Kingdom – sequence: 3 givenname: Lou surname: Ellis fullname: Ellis, Lou organization: Rheumatology Research Group, Department of Medicine, University of Cambridge, Cambridge, United Kingdom – sequence: 4 givenname: Timothy J surname: Fitzmaurice fullname: Fitzmaurice, Timothy J organization: Rheumatology Research Group, Department of Medicine, University of Cambridge, Cambridge, United Kingdom – sequence: 5 givenname: Matthew J surname: Elder fullname: Elder, Matthew J organization: Rheumatology Research Group, Department of Medicine, University of Cambridge, Cambridge, United Kingdom – sequence: 6 givenname: Nelson O surname: Gekara fullname: Gekara, Nelson O organization: Molecular Infection Medicine Sweden, Umeå Centre for Microbial Research, Department of Molecular Biology, Umeå University, Umeå, Sweden – sequence: 7 givenname: Panagiotis surname: Tourlomousis fullname: Tourlomousis, Panagiotis organization: Department of Veterinary Medicine, University of Cambridge, Cambridge, United Kingdom – sequence: 8 givenname: Clare orcidid: 0000-0002-2924-0038 surname: Bryant fullname: Bryant, Clare organization: Department of Veterinary Medicine, University of Cambridge, Cambridge, United Kingdom – sequence: 9 givenname: Simon surname: Clare fullname: Clare, Simon organization: Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, United Kingdom – sequence: 10 givenname: Ronnie surname: Chee fullname: Chee, Ronnie organization: Department of Immunology, Royal Free Hospital, London, United Kingdom – sequence: 11 givenname: Hill J S surname: Gaston fullname: Gaston, Hill J S organization: Rheumatology Research Group, Department of Medicine, University of Cambridge, Cambridge, United Kingdom – sequence: 12 givenname: Jane C surname: Goodall fullname: Goodall, Jane C organization: Rheumatology Research Group, Department of Medicine, University of Cambridge, Cambridge, United Kingdom |
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| ContentType | Journal Article |
| Copyright | COPYRIGHT 2017 Public Library of Science 2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: infection. PLoS Pathog 13(6): e1006383. https://doi.org/10.1371/journal.ppat.1006383 2017 Webster et al 2017 Webster et al 2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: infection. PLoS Pathog 13(6): e1006383. https://doi.org/10.1371/journal.ppat.1006383 |
| Copyright_xml | – notice: COPYRIGHT 2017 Public Library of Science – notice: 2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: infection. PLoS Pathog 13(6): e1006383. https://doi.org/10.1371/journal.ppat.1006383 – notice: 2017 Webster et al 2017 Webster et al – notice: 2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: infection. PLoS Pathog 13(6): e1006383. https://doi.org/10.1371/journal.ppat.1006383 |
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| DOI | 10.1371/journal.ppat.1006383 |
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| PublicationDate_xml | – month: 06 year: 2017 text: 2017-06-01 day: 01 |
| PublicationDecade | 2010 |
| PublicationPlace | United States |
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| PublicationTitle | PLoS pathogens |
| PublicationTitleAlternate | PLoS Pathog |
| PublicationYear | 2017 |
| Publisher | Public Library of Science Public Library of Science (PLoS) |
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| SubjectTerms | Activation AMP Animals Apoptosis Arthritis Assaying Attenuation Bacteria Bacterial infections Biology and Life Sciences Bone marrow Care and treatment Cell death Chlamydia Chlamydia infections Chlamydia Infections - immunology Chlamydia Infections - microbiology Chlamydia trachomatis Chlamydia trachomatis - genetics Chlamydia trachomatis - immunology Chlamydia trachomatis - physiology Colleges & universities Condoms Cyclic AMP - immunology Dendritic cells Dendritic Cells - immunology Dendritic Cells - microbiology Dosage and administration Enzyme-linked immunosorbent assay Female Health aspects Humans Immune response Immune system Immunoblotting Infections Infectious diseases Inflammasomes Inflammasomes - immunology Inflammation Innate immunity Interferon Interferon Type I - genetics Interferon Type I - immunology Interleukin 1 Interleukin-1beta - genetics Interleukin-1beta - immunology Macrophages Macrophages - immunology Macrophages - microbiology Male Medicine and Health Sciences Membrane Proteins - genetics Membrane Proteins - immunology Metabolism Metabolites Mice Microorganisms Monocytes NAD(P)H oxidase Nucleotidyltransferases - genetics Nucleotidyltransferases - immunology Oxidase Pathogens Physiological aspects Proteins Pyroptosis Replication Research and Analysis Methods Rheumatology Risk factors Sexually transmitted diseases STD Veterinary medicine |
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| Title | Detection of a microbial metabolite by STING regulates inflammasome activation in response to Chlamydia trachomatis infection |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/28570638 https://www.proquest.com/docview/1919514635/abstract/ https://search.proquest.com/docview/1905738417 https://pubmed.ncbi.nlm.nih.gov/PMC5453623 https://urn.kb.se/resolve?urn=urn:nbn:se:umu:diva-137812 https://doaj.org/article/cc7ab21c35704bf99075bec68f1688a5 http://dx.doi.org/10.1371/journal.ppat.1006383 |
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