A role for the NLRP3 inflammasome in metabolic diseases—did Warburg miss inflammation? (original) (raw)

• Hotamisligil, G.S. Inflammation and metabolic disorders. Nature 444, 860–867 (2006).
  Article CAS PubMed Google Scholar
• Fève, B. & Bastard, J.P. The role of interleukins in insulin resistance and type 2 diabetes mellitus. Nat. Rev. Endocrinol. 5, 305–311 (2009).
  PubMed Google Scholar
• Arend, W.P., Palmer, G. & Gabay, C. IL-1, IL-18, and IL-33 families of cytokines. Immunol. Rev. 223, 20–38 (2008).
  CAS PubMed Google Scholar
• Larsen, C.M. et al. Interleukin-1-receptor antagonist in type 2 diabetes mellitus. N. Engl. J. Med. 356, 1517–1526 (2007).
  Article CAS PubMed Google Scholar
• Stanley, T.L. et al. TNF-α antagonism with etanercept decreases glucose and increases the proportion of high molecular weight adiponectin in obese subjects with features of the metabolic syndrome. J. Clin. Endocrinol. Metab. 96, E146–E150 (2011).
  CAS PubMed Google Scholar
• Gonzalez-Gay, M.A., Gonzalez-Juanatey, C., Vazquez-Rodriguez, T.R., Miranda-Filloy, J.A. & Llorca, J. Insulin resistance in rheumatoid arthritis: the impact of the anti-TNF-α therapy. Ann. NY Acad. Sci. 1193, 153–159 (2010).
  CAS PubMed Google Scholar
• Solomon, D.H. et al. Association between disease-modifying antirheumatic drugs and diabetes risk in patients with rheumatoid arthritis and psoriasis. J. Am. Med. Assoc. 305, 2525–2531 (2011).
  CAS Google Scholar
• Schroder, K. & Tschopp, J. The inflammasomes. Cell 140, 821–832 (2010).
  CAS PubMed Google Scholar
• Barker, B.R., Taxman, D.J. & Ting, J.P. Cross-regulation between the IL-1β/IL-18 processing inflammasome and other inflammatory cytokines. Curr. Opin. Immunol. 23, 591–597 (2011).
  CAS PubMed PubMed Central Google Scholar
• Zhou, R., Tardivel, A., Thorens, B., Choi, I. & Tschopp, J. Thioredoxin-interacting protein links oxidative stress to inflammasome activation. Nat. Immunol. 11, 136–140 (2010).
  CAS PubMed Google Scholar
• Stienstra, R. et al. The inflammasome-mediated caspase-1 activation controls adipocyte differentiation and insulin sensitivity. Cell Metab. 12, 593–605 (2010).
  CAS PubMed PubMed Central Google Scholar
• Vandanmagsar, B. et al. The NLRP3 inflammasome instigates obesity-induced inflammation and insulin resistance. Nat. Med. 17, 179–188 (2011).
  CAS PubMed PubMed Central Google Scholar
• Wen, H. et al. Fatty acid-induced NLRP3-ASC inflammasome activation interferes with insulin signaling. Nat. Immunol. 12, 408–415 (2011).
  CAS PubMed PubMed Central Google Scholar
• Stienstra, R. et al. Inflammasome is a central player in the induction of obesity and insulin resistance. Proc. Natl. Acad. Sci. USA 108, 15324–15329 (2011).
  CAS PubMed PubMed Central Google Scholar
• Lamkanfi, M. et al. Glyburide inhibits the cryopyrin/Nalp3 inflammasome. J. Cell Biol. 187, 61–70 (2009).
  CAS PubMed PubMed Central Google Scholar
• Mandrup-Poulsen, T., Pickersgill, L. & Donath, M.Y. Blockade of interleukin 1 in type 1 diabetes mellitus. Nat. Rev. Endocrinol. 6, 158–166 (2010).
  CAS PubMed Google Scholar
• Masters, S.L. et al. Activation of the NLRP3 inflammasome by islet amyloid polypeptide provides a mechanism for enhanced IL-1β in type 2 diabetes. Nat. Immunol. 11, 897–904 (2010).
  CAS PubMed PubMed Central Google Scholar
• Westermark, P., Andersson, A. & Westermark, G.T. Islet amyloid polypeptide, islet amyloid, and diabetes mellitus. Physiol. Rev. 91, 795–826 (2011).
  CAS PubMed Google Scholar
• Maedler, K. et al. Glucose-induced beta cell production of IL-1β contributes to glucotoxicity in human pancreatic islets. J. Clin. Invest. 110, 851–860 (2002).
  CAS PubMed PubMed Central Google Scholar
• Levine, B., Mizushima, N. & Virgin, H.W. Autophagy in immunity and inflammation. Nature 469, 323–335 (2011).
  CAS PubMed PubMed Central Google Scholar
• The Wellcome Trust Case Control Consortium. Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls. Nature 447, 661–678 (2007).
• Rioux, J.D. et al. Genome-wide association study identifies new susceptibility loci for Crohn disease and implicates autophagy in disease pathogenesis. Nat. Genet. 39, 596–604 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Hampe, J. et al. A genome-wide association scan of nonsynonymous SNPs identifies a susceptibility variant for Crohn disease in ATG16L1. Nat. Genet. 39, 207–211 (2007).
  Article CAS PubMed Google Scholar
• Cadwell, K. et al. Virus-plus-susceptibility gene interaction determines Crohn's disease gene Atg16L1 phenotypes in intestine. Cell 141, 1135–1145 (2010).
  CAS PubMed PubMed Central Google Scholar
• Saitoh, T. et al. Loss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1β production. Nature 456, 264–268 (2008).
  CAS PubMed Google Scholar
• Nakahira, K. et al. Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat. Immunol. 12, 222–230 (2011).
  Article CAS PubMed Google Scholar
• Zhou, R., Yazdi, A.S., Menu, P. & Tschopp, J. A role for mitochondria in NLRP3 inflammasome activation. Nature 469, 221–225 (2011).
  CAS PubMed Google Scholar
• Yang, L., Li, P., Fu, S., Calay, E.S. & Hotamisligil, G.S. Defective hepatic autophagy in obesity promotes ER stress and causes insulin resistance. Cell Metab. 11, 467–478 (2010).
  CAS PubMed PubMed Central Google Scholar
• Kim, J., Kundu, M., Viollet, B. & Guan, K.L. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat. Cell Biol. 13, 132–141 (2011).
  CAS PubMed PubMed Central Google Scholar
• Egan, D.F. et al. Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy. Science 331, 456–461 (2011).
  CAS PubMed Google Scholar
• Davis, B.K., Wen, H. & Ting, J.P. The inflammasome NLRs in immunity, inflammation, and associated diseases. Annu. Rev. Immunol. 29, 707–735 (2011).
  CAS PubMed PubMed Central Google Scholar
• Chung, Y. et al. Critical regulation of early Th17 cell differentiation by interleukin-1 signaling. Immunity 30, 576–587 (2009).
  CAS PubMed PubMed Central Google Scholar
• Robinson, D. et al. IGIF does not drive Th1 development but synergizes with IL-12 for interferon-gamma production and activates IRAK and NFκB. Immunity 7, 571–581 (1997).
  CAS PubMed Google Scholar
• Wilson, N.J. et al. Development, cytokine profile and function of human interleukin 17-producing helper T cells. Nat. Immunol. 8, 950–957 (2007).
  CAS PubMed Google Scholar
• Acosta-Rodriguez, E.V., Napolitani, G., Lanzavecchia, A. & Sallusto, F. Interleukins 1β and 6 but not transforming growth factor-β are essential for the differentiation of interleukin 17-producing human T helper cells. Nat. Immunol. 8, 942–949 (2007).
  CAS PubMed Google Scholar
• Feuerer, M. et al. Lean, but not obese, fat is enriched for a unique population of regulatory T cells that affect metabolic parameters. Nat. Med. 15, 930–939 (2009).
  CAS PubMed PubMed Central Google Scholar
• Nishimura, S. et al. CD8+ effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity. Nat. Med. 15, 914–920 (2009).
  CAS PubMed Google Scholar
• Winer, S. et al. Normalization of obesity-associated insulin resistance through immunotherapy. Nat. Med. 15, 921–929 (2009).
  CAS PubMed PubMed Central Google Scholar
• Yang, H. et al. Obesity increases the production of proinflammatory mediators from adipose tissue T cells and compromises TCR repertoire diversity: implications for systemic inflammation and insulin resistance. J. Immunol. 185, 1836–1845 (2010).
  CAS PubMed Google Scholar
• Winer, D.A. et al. B cells promote insulin resistance through modulation of T cells and production of pathogenic IgG antibodies. Nat. Med. 17, 610–617 (2011).
  CAS PubMed PubMed Central Google Scholar
• Binder, C.J. et al. Innate and acquired immunity in atherogenesis. Nat. Med. 8, 1218–1226 (2002).
  CAS PubMed Google Scholar
• Hansson, G.K. Inflammation, atherosclerosis, and coronary artery disease. N. Engl. J. Med. 352, 1685–1695 (2005).
  CAS PubMed Google Scholar
• Kirii, H. et al. Lack of interleukin-1β decreases the severity of atherosclerosis in ApoE-deficient mice. Arterioscler. Thromb. Vasc. Biol. 23, 656–660 (2003).
  CAS PubMed Google Scholar
• Elhage, R. et al. Differential effects of interleukin-1 receptor antagonist and tumor necrosis factor binding protein on fatty-streak formation in apolipoprotein E-deficient mice. Circulation 97, 242–244 (1998).
  CAS PubMed Google Scholar
• Sabio, G. et al. A stress signaling pathway in adipose tissue regulates hepatic insulin resistance. Science 322, 1539–1543 (2008).
  CAS PubMed PubMed Central Google Scholar
• Ellingsgaard, H. et al. Interleukin-6 enhances insulin secretion by increasing glucagon-like peptide-1 secretion from L cells and α cells. Nat. Med. 17, 1481–1489 (2011).
  CAS PubMed PubMed Central Google Scholar
• Duewell, P. et al. NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature 464, 1357–1361 (2010).
  CAS PubMed PubMed Central Google Scholar
• Rajamäki, K. et al. Cholesterol crystals activate the NLRP3 inflammasome in human macrophages: a novel link between cholesterol metabolism and inflammation. PLoS ONE 5, e11765 (2010).
  PubMed PubMed Central Google Scholar
• Martinon, F., Petrilli, V., Mayor, A., Tardivel, A. & Tschopp, J. Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 440, 237–241 (2006).
  CAS PubMed Google Scholar
• Dostert, C. et al. Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science 320, 674–677 (2008).
  CAS PubMed PubMed Central Google Scholar
• Hornung, V. et al. Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat. Immunol. 9, 847–856 (2008).
  CAS PubMed PubMed Central Google Scholar
• Eisenbarth, S.C., Colegio, O.R., O'Connor, W., Sutterwala, F.S. & Flavell, R.A. Crucial role for the Nalp3 inflammasome in the immunostimulatory properties of aluminium adjuvants. Nature 453, 1122–1126 (2008).
  CAS PubMed PubMed Central Google Scholar
• Menu, P. et al. Atherosclerosis in ApoE-deficient mice progresses independently of the NLRP3 inflammasome. Cell Death Dis. 2, e137 (2011).
  CAS PubMed PubMed Central Google Scholar
• Allen, I.C. et al. The NLRP3 inflammasome functions as a negative regulator of tumorigenesis during colitis-associated cancer. J. Exp. Med. 207, 1045–1056 (2010).
  CAS PubMed PubMed Central Google Scholar
• Zaki, M.H. et al. The NLRP3 inflammasome protects against loss of epithelial integrity and mortality during experimental colitis. Immunity 32, 379–391 (2010).
  CAS PubMed PubMed Central Google Scholar
• Rock, K.L., Latz, E., Ontiveros, F. & Kono, H. The sterile inflammatory response. Annu. Rev. Immunol. 28, 321–342 (2010).
  CAS PubMed PubMed Central Google Scholar
• So, A., De Smedt, T., Revaz, S. & Tschopp, J. A pilot study of IL-1 inhibition by anakinra in acute gout. Arthritis Res. Ther. 9, R28 (2007).
  PubMed PubMed Central Google Scholar
• Terkeltaub, R. et al. The interleukin 1 inhibitor rilonacept in treatment of chronic gouty arthritis: results of a placebo-controlled, monosequence crossover, non-randomised, single-blind pilot study. Ann. Rheum. Dis. 68, 1613–1617 (2009).
  CAS PubMed Google Scholar
• So, A. et al. Canakinumab for the treatment of acute flares in difficult-to-treat gouty arthritis: Results of a multicenter, phase II, dose-ranging study. Arthritis Rheum. 62, 3064–3076 (2010).
  CAS PubMed Google Scholar
• Schlesinger, N. et al. Canakinumab reduces the risk of acute gouty arthritis flares during initiation of allopurinol treatment: results of a double-blind, randomised study. Ann. Rheum. Dis. 70, 1264–1271 (2011).
  CAS PubMed Google Scholar
• Labbé, K., McIntire, C.R., Doiron, K., Leblanc, P.M. & Saleh, M. Cellular inhibitors of apoptosis proteins cIAP1 and cIAP2 are required for efficient caspase-1 activation by the inflammasome. Immunity 35, 897–907 (2011).
  PubMed Google Scholar
• Kofoed, E.M. & Vance, R.E. Innate immune recognition of bacterial ligands by NAIPs determines inflammasome specificity. Nature 477, 592–595 (2011).
  CAS PubMed PubMed Central Google Scholar
• Sander, L.E. et al. Detection of prokaryotic mRNA signifies microbial viability and promotes immunity. Nature 474, 385–389 (2011).
  CAS PubMed PubMed Central Google Scholar
• Poeck, H. et al. Recognition of RNA virus by RIG-I results in activation of CARD9 and inflammasome signaling for interleukin 1β production. Nat. Immunol. 11, 63–69 (2010).
  CAS PubMed Google Scholar
• Conti, B.J. et al. CATERPILLER 16.2 (CLR16.2), a novel NBD/LRR family member that negatively regulates T cell function. J. Biol. Chem. 280, 18375–18385 (2005).
  CAS PubMed Google Scholar
• Allen, I.C. et al. The NLRP3 inflammasome mediates in vivo innate immunity to influenza A virus through recognition of viral RNA. Immunity 30, 556–565 (2009).
  CAS PubMed PubMed Central Google Scholar
• Bauernfeind, F. et al. Cutting edge: reactive oxygen species inhibitors block priming, but not activation, of the NLRP3 inflammasome. J. Immunol. 187, 613–617 (2011).
  CAS PubMed Google Scholar
• Kool, M. et al. An unexpected role for uric acid as an inducer of T helper 2 cell immunity to inhaled antigens and inflammatory mediator of allergic asthma. Immunity 34, 527–540 (2011).
  CAS PubMed Google Scholar
• Kuroda, E. et al. Silica crystals and aluminum salts regulate the production of prostaglandin in macrophages via NALP3 inflammasome-independent mechanisms. Immunity 34, 514–526 (2011).
  CAS PubMed Google Scholar
• Krawczyk, C.M. et al. Toll-like receptor-induced changes in glycolytic metabolism regulate dendritic cell activation. Blood 115, 4742–4749 (2010).
  CAS PubMed PubMed Central Google Scholar
• Hsu, P.P. & Sabatini, D.M. Cancer cell metabolism: Warburg and beyond. Cell 134, 703–707 (2008).
  CAS PubMed Google Scholar
• Tannahill, G.M. & O'Neill, L.A. The emerging role of metabolic regulation in the functioning of Toll-like receptors and the NOD-like receptor Nlrp3. FEBS Lett. 585, 1568–1572 (2011).
  CAS PubMed Google Scholar
• Kroemer, G. & Pouyssegur, J. Tumor cell metabolism: cancer's Achilles' heel. Cancer Cell 13, 472–482 (2008).
  CAS PubMed Google Scholar
• Christofk, H.R. et al. The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth. Nature 452, 230–233 (2008).
  CAS PubMed Google Scholar
• Luo, W. et al. Pyruvate kinase M2 is a PHD3-stimulated coactivator for hypoxia-inducible factor 1. Cell 145, 732–744 (2011).
  CAS PubMed PubMed Central Google Scholar
• Pouysségur, J., Dayan, F. & Mazure, N.M. Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature 441, 437–443 (2006).
  PubMed Google Scholar
• Cramer, T. et al. HIF-1α is essential for myeloid cell-mediated inflammation. Cell 112, 645–657 (2003).
  CAS PubMed PubMed Central Google Scholar
• Rodríguez-Prados, J.C. et al. Substrate fate in activated macrophages: a comparison between innate, classic, and alternative activation. J. Immunol. 185, 605–614 (2010).
  PubMed Google Scholar
• Peyssonnaux, C. et al. Cutting edge: Essential role of hypoxia inducible factor-1α in development of lipopolysaccharide-induced sepsis. J. Immunol. 178, 7516–7519 (2007).
  CAS PubMed Google Scholar
• Calvano, S.E. et al. A network-based analysis of systemic inflammation in humans. Nature 437, 1032–1037 (2005).
  CAS PubMed Google Scholar
• Selak, M.A. et al. Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-α prolyl hydroxylase. Cancer Cell 7, 77–85 (2005).
  CAS PubMed Google Scholar
• Nishi, K. et al. LPS induces hypoxia-inducible factor 1 activation in macrophage-differentiated cells in a reactive oxygen species-dependent manner. Antioxid. Redox Signal. 10, 983–995 (2008).
  CAS PubMed Google Scholar
• Pistollato, F. et al. Hypoxia and succinate antagonize 2-deoxyglucose effects on glioblastoma. Biochem. Pharmacol. 80, 1517–1527 (2010).
  CAS PubMed Google Scholar
• Garedew, A., Henderson, S.O. & Moncada, S. Activated macrophages utilize glycolytic ATP to maintain mitochondrial membrane potential and prevent apoptotic cell death. Cell Death Differ. 17, 1540–1550 (2010).
  CAS PubMed Google Scholar
• Dang, E.V. et al. Control of TH17/Treg balance by hypoxia-inducible factor 1. Cell 146, 772–784 (2011).
  CAS PubMed PubMed Central Google Scholar
• Shi, L.Z. et al. HIF1α-dependent glycolytic pathway orchestrates a metabolic checkpoint for the differentiation of TH17 and Treg cells. J. Exp. Med. 208, 1367–1376 (2011).
  CAS PubMed PubMed Central Google Scholar
• Emanuelli, B., Glondu, M., Filloux, C., Peraldi, P. & Van Obberghen, E. The potential role of SOCS-3 in the interleukin-1β-induced desensitization of insulin signaling in pancreatic beta-cells. Diabetes 53 Suppl 3, S97–S103 (2004).
  CAS PubMed Google Scholar
• Tilg, H. & Moschen, A.R. Inflammatory mechanisms in the regulation of insulin resistance. Mol. Med. 14, 222–231 (2008).
  CAS PubMed PubMed Central Google Scholar