Succinate is an inflammatory signal that induces IL-1β through HIF-1α
Succinate is identified as a metabolite in innate immune signalling, which leads to enhanced interleukin-1β production during inflammation. Succinate is an innate immunity signal The bacterial endotoxin lipopolysaccharide activates macrophages, as part of the innate immunity response, by inducing a...
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| Vydáno v: | Nature (London) Ročník 496; číslo 7444; s. 238 - 242 |
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| Hlavní autoři: | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Médium: | Journal Article |
| Jazyk: | angličtina |
| Vydáno: |
London
Nature Publishing Group UK
11.04.2013
Nature Publishing Group |
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| ISSN: | 0028-0836, 1476-4687, 1476-4687 |
| On-line přístup: | Získat plný text |
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| Abstract | Succinate is identified as a metabolite in innate immune signalling, which leads to enhanced interleukin-1β production during inflammation.
Succinate is an innate immunity signal
The bacterial endotoxin lipopolysaccharide activates macrophages, as part of the innate immunity response, by inducing a shift from oxidative to glycolytic metabolism. Gillian Tannahill
et al
. show here that lipopolysaccharide increases levels of the tricarboxylic acid cycle intermediate succinate in macrophages through a metabolic process not previously reported in macrophages, the 'GABA shunt'. Succinate in turn drives the key pro-inflammatory cytokine interleukin-1β.
Macrophages activated by the Gram-negative bacterial product lipopolysaccharide switch their core metabolism from oxidative phosphorylation to glycolysis
1
. Here we show that inhibition of glycolysis with 2-deoxyglucose suppresses lipopolysaccharide-induced interleukin-1β but not tumour-necrosis factor-α in mouse macrophages. A comprehensive metabolic map of lipopolysaccharide-activated macrophages shows upregulation of glycolytic and downregulation of mitochondrial genes, which correlates directly with the expression profiles of altered metabolites. Lipopolysaccharide strongly increases the levels of the tricarboxylic-acid cycle intermediate succinate. Glutamine-dependent anerplerosis is the principal source of succinate, although the ‘GABA (γ-aminobutyric acid) shunt’ pathway also has a role. Lipopolysaccharide-induced succinate stabilizes hypoxia-inducible factor-1α, an effect that is inhibited by 2-deoxyglucose, with interleukin-1β as an important target. Lipopolysaccharide also increases succinylation of several proteins. We therefore identify succinate as a metabolite in innate immune signalling, which enhances interleukin-1β production during inflammation. |
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| AbstractList | Macrophages activated by the Gram-negative bacterial product lipopolysaccharide switch their core metabolism from oxidative phosphorylation to glycolysis. Here we show that inhibition of glycolysis with 2-deoxyglucose suppresses lipopolysaccharide-induced interleukin-1β but not tumour-necrosis factor-α in mouse macrophages. A comprehensive metabolic map of lipopolysaccharide-activated macrophages shows upregulation of glycolytic and downregulation of mitochondrial genes, which correlates directly with the expression profiles of altered metabolites. Lipopolysaccharide strongly increases the levels of the tricarboxylic-acid cycle intermediate succinate. Glutamine-dependent anerplerosis is the principal source of succinate, although the 'GABA (γ-aminobutyric acid) shunt' pathway also has a role. Lipopolysaccharide-induced succinate stabilizes hypoxia-inducible factor-1α, an effect that is inhibited by 2-deoxyglucose, with interleukin-1β as an important target. Lipopolysaccharide also increases succinylation of several proteins. We therefore identify succinate as a metabolite in innate immune signalling, which enhances interleukin-1β production during inflammation.Macrophages activated by the Gram-negative bacterial product lipopolysaccharide switch their core metabolism from oxidative phosphorylation to glycolysis. Here we show that inhibition of glycolysis with 2-deoxyglucose suppresses lipopolysaccharide-induced interleukin-1β but not tumour-necrosis factor-α in mouse macrophages. A comprehensive metabolic map of lipopolysaccharide-activated macrophages shows upregulation of glycolytic and downregulation of mitochondrial genes, which correlates directly with the expression profiles of altered metabolites. Lipopolysaccharide strongly increases the levels of the tricarboxylic-acid cycle intermediate succinate. Glutamine-dependent anerplerosis is the principal source of succinate, although the 'GABA (γ-aminobutyric acid) shunt' pathway also has a role. Lipopolysaccharide-induced succinate stabilizes hypoxia-inducible factor-1α, an effect that is inhibited by 2-deoxyglucose, with interleukin-1β as an important target. Lipopolysaccharide also increases succinylation of several proteins. We therefore identify succinate as a metabolite in innate immune signalling, which enhances interleukin-1β production during inflammation. Macrophages activated by the Gram-negative bacterial product lipopolysaccharide switch their core metabolism from oxidative phosphorylation to glycolysis. Here we show that inhibition of glycolysis with 2-deoxyglucose suppresses lipopolysaccharide-induced interleukin-1β but not tumour-necrosis factor-α in mouse macrophages. A comprehensive metabolic map of lipopolysaccharide-activated macrophages shows upregulation of glycolytic and downregulation of mitochondrial genes, which correlates directly with the expression profiles of altered metabolites. Lipopolysaccharide strongly increases the levels of the tricarboxylic-acid cycle intermediate succinate. Glutamine-dependent anerplerosis is the principal source of succinate, although the 'GABA (γ-aminobutyric acid) shunt' pathway also has a role. Lipopolysaccharide-induced succinate stabilizes hypoxia-inducible factor-1α, an effect that is inhibited by 2-deoxyglucose, with interleukin-1β as an important target. Lipopolysaccharide also increases succinylation of several proteins. We therefore identify succinate as a metabolite in innate immune signalling, which enhances interleukin-1β production during inflammation. Succinate is identified as a metabolite in innate immune signalling, which leads to enhanced interleukin-1β production during inflammation. Succinate is an innate immunity signal The bacterial endotoxin lipopolysaccharide activates macrophages, as part of the innate immunity response, by inducing a shift from oxidative to glycolytic metabolism. Gillian Tannahill et al . show here that lipopolysaccharide increases levels of the tricarboxylic acid cycle intermediate succinate in macrophages through a metabolic process not previously reported in macrophages, the 'GABA shunt'. Succinate in turn drives the key pro-inflammatory cytokine interleukin-1β. Macrophages activated by the Gram-negative bacterial product lipopolysaccharide switch their core metabolism from oxidative phosphorylation to glycolysis 1 . Here we show that inhibition of glycolysis with 2-deoxyglucose suppresses lipopolysaccharide-induced interleukin-1β but not tumour-necrosis factor-α in mouse macrophages. A comprehensive metabolic map of lipopolysaccharide-activated macrophages shows upregulation of glycolytic and downregulation of mitochondrial genes, which correlates directly with the expression profiles of altered metabolites. Lipopolysaccharide strongly increases the levels of the tricarboxylic-acid cycle intermediate succinate. Glutamine-dependent anerplerosis is the principal source of succinate, although the ‘GABA (γ-aminobutyric acid) shunt’ pathway also has a role. Lipopolysaccharide-induced succinate stabilizes hypoxia-inducible factor-1α, an effect that is inhibited by 2-deoxyglucose, with interleukin-1β as an important target. Lipopolysaccharide also increases succinylation of several proteins. We therefore identify succinate as a metabolite in innate immune signalling, which enhances interleukin-1β production during inflammation. |
| Audience | Academic |
| Author | O’Neill, L. A. J. Cummins, E. Nizet, V. Xavier, R. J. Tannahill, G. M. Bernard, N. J. Goel, G. Gardet, A. Foley, N. H. Kelly, B. Masters, S. L. Corr, S. C. Auron, P. E. Kelly, V. P. Walmsley, S. Lin, H. Gottlieb, E. Pierce, K. Curtis, A. M. Whyte, M. Haneklaus, M. McGettrick, A. F. Frezza, C. Palsson-McDermott, E. M. Jany, S. S. Zheng, L. Clish, C. Adamik, J. Beasley, F. C. Tong, Z. Caffrey, B. E. Taylor, C. T. |
| Author_xml | – sequence: 1 givenname: G. M. surname: Tannahill fullname: Tannahill, G. M. organization: School of Biochemistry and Immunology, Trinity Biomedical Sciences Institute, Trinity College Dublin, Dublin 2, Ireland – sequence: 2 givenname: A. M. surname: Curtis fullname: Curtis, A. M. organization: School of Biochemistry and Immunology, Trinity Biomedical Sciences Institute, Trinity College Dublin, Dublin 2, Ireland – sequence: 3 givenname: J. surname: Adamik fullname: Adamik, J. organization: Department of Biological Sciences, Duquesne University – sequence: 4 givenname: E. M. surname: Palsson-McDermott fullname: Palsson-McDermott, E. M. organization: School of Biochemistry and Immunology, Trinity Biomedical Sciences Institute, Trinity College Dublin, Dublin 2, Ireland – sequence: 5 givenname: A. F. surname: McGettrick fullname: McGettrick, A. F. organization: School of Biochemistry and Immunology, Trinity Biomedical Sciences Institute, Trinity College Dublin, Dublin 2, Ireland – sequence: 6 givenname: G. surname: Goel fullname: Goel, G. organization: Centre for Computational and Integrative Biology, Massachusetts General Hospital, Richard B. Simches Research Center – sequence: 7 givenname: C. surname: Frezza fullname: Frezza, C. organization: Apoptosis and Tumour Physiology Laboratory, The Beatson Institute for Cancer Research, Bearsden, Glasgow G61 1BD, UK, Medical Research Council Cancer Cell Unit Hutchison/MRC Research Centre, Hills Road, Cambridge CB2 0X2, UK – sequence: 8 givenname: N. J. surname: Bernard fullname: Bernard, N. J. organization: School of Biochemistry and Immunology, Trinity Biomedical Sciences Institute, Trinity College Dublin, Dublin 2, Ireland – sequence: 9 givenname: B. surname: Kelly fullname: Kelly, B. organization: School of Biochemistry and Immunology, Trinity Biomedical Sciences Institute, Trinity College Dublin, Dublin 2, Ireland – sequence: 10 givenname: N. H. surname: Foley fullname: Foley, N. H. organization: School of Biochemistry and Immunology, Trinity Biomedical Sciences Institute, Trinity College Dublin, Dublin 2, Ireland – sequence: 11 givenname: L. surname: Zheng fullname: Zheng, L. organization: Apoptosis and Tumour Physiology Laboratory, The Beatson Institute for Cancer Research, Bearsden, Glasgow G61 1BD, UK – sequence: 12 givenname: A. surname: Gardet fullname: Gardet, A. organization: The Broad Institute of MIT and Harvard, 7 Cambridge Center – sequence: 13 givenname: Z. surname: Tong fullname: Tong, Z. organization: Department of Chemistry and Chemical Biology, Cornell University – sequence: 14 givenname: S. S. surname: Jany fullname: Jany, S. S. organization: School of Biochemistry and Immunology, Trinity Biomedical Sciences Institute, Trinity College Dublin, Dublin 2, Ireland – sequence: 15 givenname: S. C. surname: Corr fullname: Corr, S. C. organization: School of Biochemistry and Immunology, Trinity Biomedical Sciences Institute, Trinity College Dublin, Dublin 2, Ireland – sequence: 16 givenname: M. surname: Haneklaus fullname: Haneklaus, M. organization: School of Biochemistry and Immunology, Trinity Biomedical Sciences Institute, Trinity College Dublin, Dublin 2, Ireland – sequence: 17 givenname: B. E. surname: Caffrey fullname: Caffrey, B. E. organization: Smurfit Institute of Genetics, Trinity College Dublin, Dublin 2, Ireland – sequence: 18 givenname: K. surname: Pierce fullname: Pierce, K. organization: The Broad Institute of MIT and Harvard, 7 Cambridge Center – sequence: 19 givenname: S. surname: Walmsley fullname: Walmsley, S. organization: Department of Infection and Immunity, Academic Unit of Respiratory Medicine, University of Sheffield, Sheffield S10 2RX, UK – sequence: 20 givenname: F. C. surname: Beasley fullname: Beasley, F. C. organization: Division of Pediatrics, V. Nizet Laboratory, Centre for Neural Circuits and Behaviour, University of California – sequence: 21 givenname: E. surname: Cummins fullname: Cummins, E. organization: Conway Institute, University College Dublin, Dublin 4, Ireland – sequence: 22 givenname: V. surname: Nizet fullname: Nizet, V. organization: Division of Pediatrics, V. Nizet Laboratory, Centre for Neural Circuits and Behaviour, University of California – sequence: 23 givenname: M. surname: Whyte fullname: Whyte, M. organization: Department of Infection and Immunity, Academic Unit of Respiratory Medicine, University of Sheffield, Sheffield S10 2RX, UK – sequence: 24 givenname: C. T. surname: Taylor fullname: Taylor, C. T. organization: Conway Institute, University College Dublin, Dublin 4, Ireland – sequence: 25 givenname: H. surname: Lin fullname: Lin, H. organization: Department of Chemistry and Chemical Biology, Cornell University – sequence: 26 givenname: S. L. surname: Masters fullname: Masters, S. L. organization: Inflammation Division, Walter and Eliza Hall Institute, 1G Royal Parade, Parkville, Victoria 3052, Australia – sequence: 27 givenname: E. surname: Gottlieb fullname: Gottlieb, E. organization: Apoptosis and Tumour Physiology Laboratory, The Beatson Institute for Cancer Research, Bearsden, Glasgow G61 1BD, UK – sequence: 28 givenname: V. P. surname: Kelly fullname: Kelly, V. P. organization: School of Biochemistry and Immunology, Trinity Biomedical Sciences Institute, Trinity College Dublin, Dublin 2, Ireland – sequence: 29 givenname: C. surname: Clish fullname: Clish, C. organization: The Broad Institute of MIT and Harvard, 7 Cambridge Center – sequence: 30 givenname: P. E. surname: Auron fullname: Auron, P. E. organization: Department of Biological Sciences, Duquesne University – sequence: 31 givenname: R. J. surname: Xavier fullname: Xavier, R. J. organization: Centre for Computational and Integrative Biology, Massachusetts General Hospital, Richard B. Simches Research Center, Medical Research Council Cancer Cell Unit Hutchison/MRC Research Centre, Hills Road, Cambridge CB2 0X2, UK – sequence: 32 givenname: L. A. J. surname: O’Neill fullname: O’Neill, L. A. J. email: laoneill@tcd.ie organization: School of Biochemistry and Immunology, Trinity Biomedical Sciences Institute, Trinity College Dublin, Dublin 2, Ireland |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/23535595$$D View this record in MEDLINE/PubMed |
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| Snippet | Succinate is identified as a metabolite in innate immune signalling, which leads to enhanced interleukin-1β production during inflammation.
Succinate is an... Macrophages activated by the Gram-negative bacterial product lipopolysaccharide switch their core metabolism from oxidative phosphorylation to glycolysis. Here... |
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| Title | Succinate is an inflammatory signal that induces IL-1β through HIF-1α |
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