The Transcription Factor STAT-1 Couples Macrophage Synthesis of 25-Hydroxycholesterol to the Interferon Antiviral Response

Recent studies suggest that the sterol metabolic network participates in the interferon (IFN) antiviral response. However, the molecular mechanisms linking IFN with the sterol network and the identity of sterol mediators remain unknown. Here we report a cellular antiviral role for macrophage product...

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Published in	Immunity (Cambridge, Mass.) Vol. 38; no. 1; pp. 106 - 118
Main Authors	Blanc, Mathieu, Hsieh, Wei Yuan, Robertson, Kevin A., Kropp, Kai A., Forster, Thorsten, Shui, Guanghou, Lacaze, Paul, Watterson, Steven, Griffiths, Samantha J., Spann, Nathanael J., Meljon, Anna, Talbot, Simon, Krishnan, Kathiresan, Covey, Douglas F., Wenk, Markus R., Craigon, Marie, Ruzsics, Zsolts, Haas, Jürgen, Angulo, Ana, Griffiths, William J., Glass, Christopher K., Wang, Yuqin, Ghazal, Peter
Format	Journal Article
Language	English
Published	United States Elsevier Inc 24.01.2013 Elsevier Limited Cell Press
Subjects	Animals Antiviral Agents - pharmacology Binding Sites Biosynthesis Bone Marrow Cells - drug effects Bone Marrow Cells - immunology Bone Marrow Cells - metabolism Bone Marrow Cells - virology Cholesterol Deoxyribonucleic acid DNA Experiments Gene Expression Regulation Genes Genomes Hydroxycholesterols - metabolism Hydroxycholesterols - pharmacology Infections Interferons - pharmacology Lipids Liver X Receptors Macrophage Activation - drug effects Macrophage Activation - immunology Macrophages - drug effects Macrophages - immunology Macrophages - metabolism Macrophages - virology Metabolism Metabolites Mevalonic Acid - metabolism Mice Orphan Nuclear Receptors - metabolism Promoter Regions, Genetic Protein Binding Regulation STAT1 Transcription Factor - metabolism Steroid Hydroxylases - genetics Sterols Transcription factors Viral infections Virus Replication - drug effects
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Abstract	Recent studies suggest that the sterol metabolic network participates in the interferon (IFN) antiviral response. However, the molecular mechanisms linking IFN with the sterol network and the identity of sterol mediators remain unknown. Here we report a cellular antiviral role for macrophage production of 25-hydroxycholesterol (cholest-5-en-3β,25-diol, 25HC) as a component of the sterol metabolic network linked to the IFN response via Stat1. By utilizing quantitative metabolome profiling of all naturally occurring oxysterols upon infection or IFN-stimulation, we reveal 25HC as the only macrophage-synthesized and -secreted oxysterol. We show that 25HC can act at multiple levels as a potent paracrine inhibitor of viral infection for a broad range of viruses. We also demonstrate, using transcriptional regulatory-network analyses, genetic interventions and chromatin immunoprecipitation experiments that Stat1 directly coupled Ch25h regulation to IFN in macrophages. Our studies describe a physiological role for 25HC as a sterol-lipid effector of an innate immune pathway. [Display omitted] ► Macrophage PRR sensing of virus or IFN activation induce 25HC synthesis and secretion ► Stat1 rapidly binds and activates the promoter of cholesterol-25-hydroxylase (Ch25h) ► 25HC exerts multilevel antiviral function for a range of different viruses ► 25HC is an intrinsic paracrine and autocrine effector of the IFN antiviral response
AbstractList	Recent studies suggest that the sterol metabolic network participates in the interferon (IFN) antiviral response. However, the molecular mechanisms linking IFN with the sterol network and the identity of sterol mediators remain unknown. Here we report a cellular antiviral role for macrophage production of 25-hydroxycholesterol (cholest-5-en-3β,25-diol, 25HC) as a component of the sterol metabolic network linked to the IFN response via Stat1. By utilizing quantitative metabolome profiling of all naturally occurring oxysterols upon infection or IFN-stimulation, we reveal 25HC as the only macrophage-synthesized and -secreted oxysterol. We show that 25HC can act at multiple levels as a potent paracrine inhibitor of viral infection for a broad range of viruses. We also demonstrate, using transcriptional regulatory-network analyses, genetic interventions and chromatin immunoprecipitation experiments that Stat1 directly coupled Ch25h regulation to IFN in macrophages. Our studies describe a physiological role for 25HC as a sterol-lipid effector of an innate immune pathway.Recent studies suggest that the sterol metabolic network participates in the interferon (IFN) antiviral response. However, the molecular mechanisms linking IFN with the sterol network and the identity of sterol mediators remain unknown. Here we report a cellular antiviral role for macrophage production of 25-hydroxycholesterol (cholest-5-en-3β,25-diol, 25HC) as a component of the sterol metabolic network linked to the IFN response via Stat1. By utilizing quantitative metabolome profiling of all naturally occurring oxysterols upon infection or IFN-stimulation, we reveal 25HC as the only macrophage-synthesized and -secreted oxysterol. We show that 25HC can act at multiple levels as a potent paracrine inhibitor of viral infection for a broad range of viruses. We also demonstrate, using transcriptional regulatory-network analyses, genetic interventions and chromatin immunoprecipitation experiments that Stat1 directly coupled Ch25h regulation to IFN in macrophages. Our studies describe a physiological role for 25HC as a sterol-lipid effector of an innate immune pathway. Recent studies suggest that the sterol metabolic network participates in the interferon (IFN) antiviral response. However, the molecular mechanisms linking IFN with the sterol network and the identity of sterol mediators remain unknown. Here we report a cellular antiviral role for macrophage production of 25-hydroxycholesterol (cholest-5-en-3 beta ,25-diol, 25HC) as a component of the sterol metabolic network linked to the IFN response via Stat1. By utilizing quantitative metabolome profiling of all naturally occurring oxysterols upon infection or IFN-stimulation, we reveal 25HC as the only macrophage-synthesized and -secreted oxysterol. We show that 25HC can act at multiple levels as a potent paracrine inhibitor of viral infection for a broad range of viruses. We also demonstrate, using transcriptional regulatory-network analyses, genetic interventions and chromatin immunoprecipitation experiments that Stat1 directly coupled regulation to IFN in macrophages. Our studies describe a physiological role for 25HC as a sterol-lipid effector of an innate immune pathway. Recent studies suggest that the sterol metabolic network participates in the interferon (IFN) antiviral response. However, the molecular mechanisms linking IFN with the sterol network and the identity of sterol mediators remain unknown. Here we report a cellular antiviral role for macrophage production of 25-hydroxycholesterol (cholest-5-en-3β,25-diol, 25HC) as a component of the sterol metabolic network linked to the IFN response via Stat1. By utilizing quantitative metabolome profiling of all naturally occurring oxysterols upon infection or IFN-stimulation, we reveal 25HC as the only macrophage-synthesized and -secreted oxysterol. We show that 25HC can act at multiple levels as a potent paracrine inhibitor of viral infection for a broad range of viruses. We also demonstrate, using transcriptional regulatory-network analyses, genetic interventions and chromatin immunoprecipitation experiments that Stat1 directly coupled Ch25h regulation to IFN in macrophages. Our studies describe a physiological role for 25HC as a sterol-lipid effector of an innate immune pathway. Recent studies suggest that the sterol metabolic network participates in the interferon (IFN) antiviral response. However, the molecular mechanisms linking IFN with the sterol network and the identity of sterol mediators remain unknown. Here we report a cellular antiviral role for macrophage production of 25-hydroxycholesterol (cholest-5-en-3β,25-diol, 25HC) as a component of the sterol metabolic network linked to the IFN response via Stat1. By utilizing quantitative metabolome profiling of all naturally occurring oxysterols upon infection or IFN-stimulation, we reveal 25HC as the only macrophage-synthesized and -secreted oxysterol. We show that 25HC can act at multiple levels as a potent paracrine inhibitor of viral infection for a broad range of viruses. We also demonstrate, using transcriptional regulatory-network analyses, genetic interventions and chromatin immunoprecipitation experiments that Stat1 directly coupled Ch25h regulation to IFN in macrophages. Our studies describe a physiological role for 25HC as a sterol-lipid effector of an innate immune pathway. Recent studies suggest that the sterol metabolic network participates in the interferon (IFN) antiviral response. However, the molecular mechanisms linking IFN with the sterol network and the identity of sterol mediators remain unknown. Here we report a cellular antiviral role for macrophage production of 25-hydroxycholesterol (cholest-5-en-3β,25-diol, 25HC) as a component of the sterol metabolic network linked to the IFN response via Stat1. By utilizing quantitative metabolome profiling of all naturally occurring oxysterols upon infection or IFN-stimulation, we reveal 25HC as the only macrophage-synthesized and -secreted oxysterol. We show that 25HC can act at multiple levels as a potent paracrine inhibitor of viral infection for a broad range of viruses. We also demonstrate, using transcriptional regulatory-network analyses, genetic interventions and chromatin immunoprecipitation experiments that Stat1 directly coupledCh25hregulation to IFN in macrophages. Our studies describe a physiological role for 25HC as a sterol-lipid effector of an innate immune pathway. Recent studies suggest that the sterol metabolic network participates in the interferon (IFN) antiviral response. However, the molecular mechanisms linking IFN with the sterol network and the identity of sterol mediators remain unknown. Here we report a cellular antiviral role for macrophage production of 25-hydroxycholesterol (cholest-5-en-3β,25-diol, 25HC) as a component of the sterol metabolic network linked to the IFN response via Stat1. By utilizing quantitative metabolome profiling of all naturally occurring oxysterols upon infection or IFN-stimulation, we reveal 25HC as the only macrophage-synthesized and -secreted oxysterol. We show that 25HC can act at multiple levels as a potent paracrine inhibitor of viral infection for a broad range of viruses. We also demonstrate, using transcriptional regulatory-network analyses, genetic interventions and chromatin immunoprecipitation experiments that Stat1 directly coupled Ch25h regulation to IFN in macrophages. Our studies describe a physiological role for 25HC as a sterol-lipid effector of an innate immune pathway. [Display omitted] ► Macrophage PRR sensing of virus or IFN activation induce 25HC synthesis and secretion ► Stat1 rapidly binds and activates the promoter of cholesterol-25-hydroxylase (Ch25h) ► 25HC exerts multilevel antiviral function for a range of different viruses ► 25HC is an intrinsic paracrine and autocrine effector of the IFN antiviral response
Author	Shui, Guanghou Hsieh, Wei Yuan Blanc, Mathieu Craigon, Marie Robertson, Kevin A. Lacaze, Paul Griffiths, William J. Watterson, Steven Haas, Jürgen Ghazal, Peter Griffiths, Samantha J. Meljon, Anna Ruzsics, Zsolts Spann, Nathanael J. Covey, Douglas F. Kropp, Kai A. Talbot, Simon Krishnan, Kathiresan Wang, Yuqin Wenk, Markus R. Forster, Thorsten Angulo, Ana Glass, Christopher K.
AuthorAffiliation	8 Facultad de Medicina, Institut d’Investigacions Biomèdiques August Pi i Sunyer, Rosselló 149-153, Barcelona 08036, Spain 3 Departments of Biochemistry and Biological Sciences, Yong Loo Lin School of Medicine, National University of Singapore, Singapore 117597 4 Department of Molecular Biology, University of California, San Diego, La Jolla, CA 92093, USA 5 Institute of Mass Spectrometry, College of Medicine, Grove Building, Swansea University, Singleton Park, Swansea SA2 8PP, UK 2 SynthSys (Synthetic and Systems Biology), University of Edinburgh, The King’s Buildings, Edinburgh EH9 3JD, UK 1 Division of Pathway Medicine and Edinburgh Infectious Diseases, University of Edinburgh, Edinburgh EH16 4SB, UK 6 Department of Developmental Biology, Washington University School of Medicine, St. Louis, MO 63011, USA 7 Max von Pettenkofer-Institut, Ludwig-Maximilians-Universität München, Genzentrum, Feodor Lynen Str. 25, 81377 Munich, Germany
AuthorAffiliation_xml	– name: 6 Department of Developmental Biology, Washington University School of Medicine, St. Louis, MO 63011, USA – name: 2 SynthSys (Synthetic and Systems Biology), University of Edinburgh, The King’s Buildings, Edinburgh EH9 3JD, UK – name: 3 Departments of Biochemistry and Biological Sciences, Yong Loo Lin School of Medicine, National University of Singapore, Singapore 117597 – name: 5 Institute of Mass Spectrometry, College of Medicine, Grove Building, Swansea University, Singleton Park, Swansea SA2 8PP, UK – name: 7 Max von Pettenkofer-Institut, Ludwig-Maximilians-Universität München, Genzentrum, Feodor Lynen Str. 25, 81377 Munich, Germany – name: 8 Facultad de Medicina, Institut d’Investigacions Biomèdiques August Pi i Sunyer, Rosselló 149-153, Barcelona 08036, Spain – name: 1 Division of Pathway Medicine and Edinburgh Infectious Diseases, University of Edinburgh, Edinburgh EH16 4SB, UK – name: 4 Department of Molecular Biology, University of California, San Diego, La Jolla, CA 92093, USA
Author_xml	– sequence: 1 givenname: Mathieu surname: Blanc fullname: Blanc, Mathieu organization: Division of Pathway Medicine and Edinburgh Infectious Diseases, University of Edinburgh, Edinburgh EH16 4SB, UK – sequence: 2 givenname: Wei Yuan surname: Hsieh fullname: Hsieh, Wei Yuan organization: Division of Pathway Medicine and Edinburgh Infectious Diseases, University of Edinburgh, Edinburgh EH16 4SB, UK – sequence: 3 givenname: Kevin A. surname: Robertson fullname: Robertson, Kevin A. organization: Division of Pathway Medicine and Edinburgh Infectious Diseases, University of Edinburgh, Edinburgh EH16 4SB, UK – sequence: 4 givenname: Kai A. surname: Kropp fullname: Kropp, Kai A. organization: Division of Pathway Medicine and Edinburgh Infectious Diseases, University of Edinburgh, Edinburgh EH16 4SB, UK – sequence: 5 givenname: Thorsten surname: Forster fullname: Forster, Thorsten organization: Division of Pathway Medicine and Edinburgh Infectious Diseases, University of Edinburgh, Edinburgh EH16 4SB, UK – sequence: 6 givenname: Guanghou surname: Shui fullname: Shui, Guanghou organization: Departments of Biochemistry and Biological Sciences, Yong Loo Lin School of Medicine, National University of Singapore, Singapore 117597 – sequence: 7 givenname: Paul surname: Lacaze fullname: Lacaze, Paul organization: Division of Pathway Medicine and Edinburgh Infectious Diseases, University of Edinburgh, Edinburgh EH16 4SB, UK – sequence: 8 givenname: Steven surname: Watterson fullname: Watterson, Steven organization: Division of Pathway Medicine and Edinburgh Infectious Diseases, University of Edinburgh, Edinburgh EH16 4SB, UK – sequence: 9 givenname: Samantha J. surname: Griffiths fullname: Griffiths, Samantha J. organization: Division of Pathway Medicine and Edinburgh Infectious Diseases, University of Edinburgh, Edinburgh EH16 4SB, UK – sequence: 10 givenname: Nathanael J. surname: Spann fullname: Spann, Nathanael J. organization: Department of Molecular Biology, University of California, San Diego, La Jolla, CA 92093, USA – sequence: 11 givenname: Anna surname: Meljon fullname: Meljon, Anna organization: Institute of Mass Spectrometry, College of Medicine, Grove Building, Swansea University, Singleton Park, Swansea SA2 8PP, UK – sequence: 12 givenname: Simon surname: Talbot fullname: Talbot, Simon organization: Division of Pathway Medicine and Edinburgh Infectious Diseases, University of Edinburgh, Edinburgh EH16 4SB, UK – sequence: 13 givenname: Kathiresan surname: Krishnan fullname: Krishnan, Kathiresan organization: Department of Developmental Biology, Washington University School of Medicine, St. Louis, MO 63011, USA – sequence: 14 givenname: Douglas F. surname: Covey fullname: Covey, Douglas F. organization: Department of Developmental Biology, Washington University School of Medicine, St. Louis, MO 63011, USA – sequence: 15 givenname: Markus R. surname: Wenk fullname: Wenk, Markus R. organization: Departments of Biochemistry and Biological Sciences, Yong Loo Lin School of Medicine, National University of Singapore, Singapore 117597 – sequence: 16 givenname: Marie surname: Craigon fullname: Craigon, Marie organization: Division of Pathway Medicine and Edinburgh Infectious Diseases, University of Edinburgh, Edinburgh EH16 4SB, UK – sequence: 17 givenname: Zsolts surname: Ruzsics fullname: Ruzsics, Zsolts organization: Max von Pettenkofer-Institut, Ludwig-Maximilians-Universität München, Genzentrum, Feodor Lynen Str. 25, 81377 Munich, Germany – sequence: 18 givenname: Jürgen surname: Haas fullname: Haas, Jürgen organization: Division of Pathway Medicine and Edinburgh Infectious Diseases, University of Edinburgh, Edinburgh EH16 4SB, UK – sequence: 19 givenname: Ana surname: Angulo fullname: Angulo, Ana organization: Facultad de Medicina, Institut d’Investigacions Biomèdiques August Pi i Sunyer, Rosselló 149-153, Barcelona 08036, Spain – sequence: 20 givenname: William J. surname: Griffiths fullname: Griffiths, William J. organization: Institute of Mass Spectrometry, College of Medicine, Grove Building, Swansea University, Singleton Park, Swansea SA2 8PP, UK – sequence: 21 givenname: Christopher K. surname: Glass fullname: Glass, Christopher K. organization: Department of Molecular Biology, University of California, San Diego, La Jolla, CA 92093, USA – sequence: 22 givenname: Yuqin surname: Wang fullname: Wang, Yuqin organization: Institute of Mass Spectrometry, College of Medicine, Grove Building, Swansea University, Singleton Park, Swansea SA2 8PP, UK – sequence: 23 givenname: Peter surname: Ghazal fullname: Ghazal, Peter email: p.ghazal@ed.ac.uk organization: Division of Pathway Medicine and Edinburgh Infectious Diseases, University of Edinburgh, Edinburgh EH16 4SB, UK
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/23273843$$D View this record in MEDLINE/PubMed
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Snippet	Recent studies suggest that the sterol metabolic network participates in the interferon (IFN) antiviral response. However, the molecular mechanisms linking IFN...
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SubjectTerms	Animals Antiviral Agents - pharmacology Binding Sites Biosynthesis Bone Marrow Cells - drug effects Bone Marrow Cells - immunology Bone Marrow Cells - metabolism Bone Marrow Cells - virology Cholesterol Deoxyribonucleic acid DNA Experiments Gene Expression Regulation Genes Genomes Hydroxycholesterols - metabolism Hydroxycholesterols - pharmacology Infections Interferons - pharmacology Lipids Liver X Receptors Macrophage Activation - drug effects Macrophage Activation - immunology Macrophages - drug effects Macrophages - immunology Macrophages - metabolism Macrophages - virology Metabolism Metabolites Mevalonic Acid - metabolism Mice Orphan Nuclear Receptors - metabolism Promoter Regions, Genetic Protein Binding Regulation STAT1 Transcription Factor - metabolism Steroid Hydroxylases - genetics Sterols Transcription factors Viral infections Virus Replication - drug effects
Title	The Transcription Factor STAT-1 Couples Macrophage Synthesis of 25-Hydroxycholesterol to the Interferon Antiviral Response
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