The Immunomodulatory Metabolite Itaconate Modifies NLRP3 and Inhibits Inflammasome Activation
The Krebs cycle-derived metabolite itaconate is highly upregulated in inflammatory macrophages and exerts immunomodulatory effects through cysteine modifications on target proteins. The NLRP3 inflammasome, which cleaves IL-1β, IL-18, and gasdermin D, must be tightly regulated to avoid excessive infl...
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| Published in | Cell metabolism Vol. 32; no. 3; pp. 468 - 478.e7 |
|---|---|
| Main Authors | , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
01.09.2020
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| Subjects | |
| Online Access | Get full text |
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| Abstract | The Krebs cycle-derived metabolite itaconate is highly upregulated in inflammatory macrophages and exerts immunomodulatory effects through cysteine modifications on target proteins. The NLRP3 inflammasome, which cleaves IL-1β, IL-18, and gasdermin D, must be tightly regulated to avoid excessive inflammation. Here we provide evidence that itaconate modifies NLRP3 and inhibits inflammasome activation. Itaconate and its derivative, 4-octyl itaconate (4-OI), inhibited NLRP3 inflammasome activation, but not AIM2 or NLRC4. Conversely, NLRP3 activation was increased in itaconate-depleted Irg1−/− macrophages. 4-OI inhibited the interaction between NLRP3 and NEK7, a key step in the activation process, and “dicarboxypropylated” C548 on NLRP3. Furthermore, 4-OI inhibited NLRP3-dependent IL-1β release from PBMCs isolated from cryopyrin-associated periodic syndrome (CAPS) patients, and reduced inflammation in an in vivo model of urate-induced peritonitis. Our results identify itaconate as an endogenous metabolic regulator of the NLRP3 inflammasome and describe a process that may be exploited therapeutically to alleviate inflammation in NLRP3-driven disorders.
[Display omitted]
•Itaconate and its derivative 4-OI (which generates itaconate) block NLRP3 activation•Itaconate-depleted Irg1−/− BMDMs exhibit increased NLRP3 inflammasome activation•4-OI “dicarboxypropylates” C548 on NLRP3 and blocks the NLRP3-NEK7 interaction•4-OI reduces peritonitis in vivo and blocks IL-1β release from CAPS patient PBMCs
Hooftman et al. reveal a role for the Krebs cycle-derived metabolite itaconate in regulating the NLRP3 inflammasome. Itaconate specifically blocks NLRP3 inflammasome activation by reducing the NLRP3-NEK7 interaction, likely due to modification of C548 on NLRP3. Furthermore, itaconate inhibits IL-1β release from cells isolated from patients with the NLRP3-mediated disease CAPS. |
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| AbstractList | The Krebs cycle-derived metabolite itaconate is highly upregulated in inflammatory macrophages and exerts immunomodulatory effects through cysteine modifications on target proteins. The NLRP3 inflammasome, which cleaves IL-1β, IL-18, and gasdermin D, must be tightly regulated to avoid excessive inflammation. Here we provide evidence that itaconate modifies NLRP3 and inhibits inflammasome activation. Itaconate and its derivative, 4-octyl itaconate (4-OI), inhibited NLRP3 inflammasome activation, but not AIM2 or NLRC4. Conversely, NLRP3 activation was increased in itaconate-depleted
Irg1
−/−
macrophages. 4-OI inhibited the interaction between NLRP3 and NEK7, a key step in the activation process, and “dicarboxypropylated” C548 on NLRP3. Furthermore, 4-OI inhibited NLRP3-dependent IL-1β release from PBMCs isolated from cryopyrin-associated periodic syndrome (CAPS) patients, and reduced inflammation in an
in vivo
model of urate-induced peritonitis. Our results identify itaconate as an endogenous metabolic regulator of the NLRP3 inflammasome and describe a process that may be exploited therapeutically to alleviate inflammation in NLRP3-driven disorders.
•
Itaconate and its derivative 4-OI (which generates itaconate) block NLRP3 activation
•
Itaconate-depleted
Irg1
−/−
BMDMs exhibit increased NLRP3 inflammasome activation
•
4-OI “dicarboxypropylates” C548 on NLRP3 and blocks the NLRP3-NEK7 interaction
•
4-OI reduces peritonitis
in vivo
and blocks IL-1β release from CAPS patient PBMCs
Hooftman et al. reveal a role for the Krebs cycle-derived metabolite itaconate in regulating the NLRP3 inflammasome. Itaconate specifically blocks NLRP3 inflammasome activation by reducing the NLRP3-NEK7 interaction, likely due to modification of C548 on NLRP3. Furthermore, itaconate inhibits IL-1β release from cells isolated from patients with the NLRP3-mediated disease CAPS. The Krebs cycle-derived metabolite itaconate is highly upregulated in inflammatory macrophages and exerts immunomodulatory effects through cysteine modifications on target proteins. The NLRP3 inflammasome, which cleaves IL-1β, IL-18, and gasdermin D, must be tightly regulated to avoid excessive inflammation. Here we provide evidence that itaconate modifies NLRP3 and inhibits inflammasome activation. Itaconate and its derivative, 4-octyl itaconate (4-OI), inhibited NLRP3 inflammasome activation, but not AIM2 or NLRC4. Conversely, NLRP3 activation was increased in itaconate-depleted Irg1-/- macrophages. 4-OI inhibited the interaction between NLRP3 and NEK7, a key step in the activation process, and "dicarboxypropylated" C548 on NLRP3. Furthermore, 4-OI inhibited NLRP3-dependent IL-1β release from PBMCs isolated from cryopyrin-associated periodic syndrome (CAPS) patients, and reduced inflammation in an in vivo model of urate-induced peritonitis. Our results identify itaconate as an endogenous metabolic regulator of the NLRP3 inflammasome and describe a process that may be exploited therapeutically to alleviate inflammation in NLRP3-driven disorders.The Krebs cycle-derived metabolite itaconate is highly upregulated in inflammatory macrophages and exerts immunomodulatory effects through cysteine modifications on target proteins. The NLRP3 inflammasome, which cleaves IL-1β, IL-18, and gasdermin D, must be tightly regulated to avoid excessive inflammation. Here we provide evidence that itaconate modifies NLRP3 and inhibits inflammasome activation. Itaconate and its derivative, 4-octyl itaconate (4-OI), inhibited NLRP3 inflammasome activation, but not AIM2 or NLRC4. Conversely, NLRP3 activation was increased in itaconate-depleted Irg1-/- macrophages. 4-OI inhibited the interaction between NLRP3 and NEK7, a key step in the activation process, and "dicarboxypropylated" C548 on NLRP3. Furthermore, 4-OI inhibited NLRP3-dependent IL-1β release from PBMCs isolated from cryopyrin-associated periodic syndrome (CAPS) patients, and reduced inflammation in an in vivo model of urate-induced peritonitis. Our results identify itaconate as an endogenous metabolic regulator of the NLRP3 inflammasome and describe a process that may be exploited therapeutically to alleviate inflammation in NLRP3-driven disorders. The Krebs cycle-derived metabolite itaconate is highly upregulated in inflammatory macrophages and exerts immunomodulatory effects through cysteine modifications on target proteins. The NLRP3 inflammasome, which cleaves IL-1β, IL-18, and gasdermin D, must be tightly regulated to avoid excessive inflammation. Here we provide evidence that itaconate modifies NLRP3 and inhibits inflammasome activation. Itaconate and its derivative, 4-octyl itaconate (4-OI), inhibited NLRP3 inflammasome activation, but not AIM2 or NLRC4. Conversely, NLRP3 activation was increased in itaconate-depleted Irg1−/− macrophages. 4-OI inhibited the interaction between NLRP3 and NEK7, a key step in the activation process, and “dicarboxypropylated” C548 on NLRP3. Furthermore, 4-OI inhibited NLRP3-dependent IL-1β release from PBMCs isolated from cryopyrin-associated periodic syndrome (CAPS) patients, and reduced inflammation in an in vivo model of urate-induced peritonitis. Our results identify itaconate as an endogenous metabolic regulator of the NLRP3 inflammasome and describe a process that may be exploited therapeutically to alleviate inflammation in NLRP3-driven disorders. [Display omitted] •Itaconate and its derivative 4-OI (which generates itaconate) block NLRP3 activation•Itaconate-depleted Irg1−/− BMDMs exhibit increased NLRP3 inflammasome activation•4-OI “dicarboxypropylates” C548 on NLRP3 and blocks the NLRP3-NEK7 interaction•4-OI reduces peritonitis in vivo and blocks IL-1β release from CAPS patient PBMCs Hooftman et al. reveal a role for the Krebs cycle-derived metabolite itaconate in regulating the NLRP3 inflammasome. Itaconate specifically blocks NLRP3 inflammasome activation by reducing the NLRP3-NEK7 interaction, likely due to modification of C548 on NLRP3. Furthermore, itaconate inhibits IL-1β release from cells isolated from patients with the NLRP3-mediated disease CAPS. The Krebs cycle-derived metabolite itaconate is highly upregulated in inflammatory macrophages and exerts immunomodulatory effects through cysteine modifications on target proteins. The NLRP3 inflammasome, which cleaves IL-1β, IL-18, and gasdermin D, must be tightly regulated to avoid excessive inflammation. Here we provide evidence that itaconate modifies NLRP3 and inhibits inflammasome activation. Itaconate and its derivative, 4-octyl itaconate (4-OI), inhibited NLRP3 inflammasome activation, but not AIM2 or NLRC4. Conversely, NLRP3 activation was increased in itaconate-depleted Irg1 macrophages. 4-OI inhibited the interaction between NLRP3 and NEK7, a key step in the activation process, and "dicarboxypropylated" C548 on NLRP3. Furthermore, 4-OI inhibited NLRP3-dependent IL-1β release from PBMCs isolated from cryopyrin-associated periodic syndrome (CAPS) patients, and reduced inflammation in an in vivo model of urate-induced peritonitis. Our results identify itaconate as an endogenous metabolic regulator of the NLRP3 inflammasome and describe a process that may be exploited therapeutically to alleviate inflammation in NLRP3-driven disorders. |
| Author | Fischer, Roman Hooftman, Alexander Corcoran, Sarah E. Banahan, Kathy O’Neill, Luke A.J. Runtsch, Marah C. Irvine, Alan D. Hughes, Mark M. Angiari, Stefano Slivka, Peter F. Ruzek, Melanie C. McGettrick, Anne F. Hester, Svenja Ling, Chris |
| Author_xml | – sequence: 1 givenname: Alexander surname: Hooftman fullname: Hooftman, Alexander organization: School of Biochemistry and Immunology, Trinity Biomedical Sciences Institute, Trinity College Dublin, Dublin 2, Ireland – sequence: 2 givenname: Stefano surname: Angiari fullname: Angiari, Stefano organization: School of Biochemistry and Immunology, Trinity Biomedical Sciences Institute, Trinity College Dublin, Dublin 2, Ireland – sequence: 3 givenname: Svenja surname: Hester fullname: Hester, Svenja organization: Nuffield Department of Medicine, Target Discovery Institute, University of Oxford, Oxford OX3 7FZ, UK – sequence: 4 givenname: Sarah E. surname: Corcoran fullname: Corcoran, Sarah E. organization: School of Biochemistry and Immunology, Trinity Biomedical Sciences Institute, Trinity College Dublin, Dublin 2, Ireland – sequence: 5 givenname: Marah C. surname: Runtsch fullname: Runtsch, Marah C. organization: School of Biochemistry and Immunology, Trinity Biomedical Sciences Institute, Trinity College Dublin, Dublin 2, Ireland – sequence: 6 givenname: Chris surname: Ling fullname: Ling, Chris organization: Mass Spectrometry, Analytical Research Technologies, Abbvie, North Chicago, IL 60064, USA – sequence: 7 givenname: Melanie C. surname: Ruzek fullname: Ruzek, Melanie C. organization: Immunology Discovery, Abbvie, Worcester, MA 01605, USA – sequence: 8 givenname: Peter F. surname: Slivka fullname: Slivka, Peter F. organization: Immunology Discovery, Abbvie, Worcester, MA 01605, USA – sequence: 9 givenname: Anne F. surname: McGettrick fullname: McGettrick, Anne F. organization: School of Biochemistry and Immunology, Trinity Biomedical Sciences Institute, Trinity College Dublin, Dublin 2, Ireland – sequence: 10 givenname: Kathy surname: Banahan fullname: Banahan, Kathy organization: School of Biochemistry and Immunology, Trinity Biomedical Sciences Institute, Trinity College Dublin, Dublin 2, Ireland – sequence: 11 givenname: Mark M. surname: Hughes fullname: Hughes, Mark M. organization: School of Biochemistry and Immunology, Trinity Biomedical Sciences Institute, Trinity College Dublin, Dublin 2, Ireland – sequence: 12 givenname: Alan D. surname: Irvine fullname: Irvine, Alan D. organization: Pediatric Dermatology, Children’s Health Ireland, Crumlin, Dublin 12, Ireland – sequence: 13 givenname: Roman surname: Fischer fullname: Fischer, Roman organization: Nuffield Department of Medicine, Target Discovery Institute, University of Oxford, Oxford OX3 7FZ, UK – sequence: 14 givenname: Luke A.J. surname: O’Neill fullname: O’Neill, Luke 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/32791101$$D View this record in MEDLINE/PubMed |
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| SubjectTerms | Animals cysteine modification IL-1β Immunologic Factors - pharmacology immunometabolism inflammasome Inflammasomes - antagonists & inhibitors Inflammasomes - metabolism itaconate macrophage metabolite Mice Mice, Inbred C57BL Mice, Knockout NEK7 NLR Family, Pyrin Domain-Containing 3 Protein - deficiency NLR Family, Pyrin Domain-Containing 3 Protein - metabolism NLRP3 pyroptosis Short Succinates - pharmacology |
| Title | The Immunomodulatory Metabolite Itaconate Modifies NLRP3 and Inhibits Inflammasome Activation |
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