NLRP3 and IL-1β in macrophages as critical regulators of metabolic diseases

Diabetes, Obesity and Metabolism

Volumn 15, Issue S3, 2013, Pages 19-25

  Mcgettrick, A F ^a   O'Neill, L A J ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

AMPK; Glycolysis; Inflammasome; Metabolic disorders; NLRP3

Indexed keywords

ADENYLATE KINASE; INFLAMMASOME; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; SALSALATE;

ATHEROSCLEROSIS; CELL ACTIVATION; FATTY ACID OXIDATION; GLUCOSE BLOOD LEVEL; GLYCOLYSIS; GOUT; HUMAN; INSULIN RESISTANCE; INSULIN SENSITIVITY; LIPID METABOLISM; MACROPHAGE; METABOLIC DISORDER; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; REVIEW;

AMPK; GLYCOLYSIS; INFLAMMASOME; METABOLIC DISORDERS; NLRP3;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CARRIER PROTEINS; GLYCOLYSIS; HUMANS; INFLAMMATION; INTERLEUKIN-1BETA; MACROPHAGES; METABOLIC DISEASES;

EID: 84883542301     PISSN: 14628902     EISSN: 14631326     Source Type: Journal    
DOI: 10.1111/dom.12169     Document Type: Review

References (75)

1. Ting JP, Lovering RC, Alnemri ES et al. The NLR gene family: a standard nomenclature. Immunity 2008; 28: 285-287.
2. Shaw PJ, McDermott MF, Kanneganti TD. Inflammasomes and autoimmunity. Trends Mol Med 2011; 17: 57-64.
3. Bryant C, Fitzgerald KA. Molecular mechanisms involved in inflammasome activation. Trends Cell Biol 2009; 19: 455-464.
4. Sims JE, Smith DE. The IL-1 family: regulators of immunity. Nat Rev Immunol 2010; 10: 89-102.
5. Ben-Sasson SZ, Hu-Li J, Quiel J et al. IL-1 acts directly on CD4 T cells to enhance their antigen-driven expansion and differentiation. Proc Nat Acad Sci U S A 2009; 106: 7119-7124.
6. Perregaux D, Gabel CA. Interleukin-1 beta maturation and release in response to ATP and nigericin. Evidence that potassium depletion mediated by these agents is a necessary and common feature of their activity. J Biol Chem 1994; 269: 15195-15203.
7. Petrilli V, Papin S, Dostert C, Mayor A, Martinon F, Tschopp J. Activation of the NALP3 inflammasome is triggered by low intracellular potassium concentration. Cell Death Differ 2007; 14: 1583-1589.
8. Dostert C, Petrilli V, Van Bruggen R, Steele C, Mossman BT, Tschopp J. Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science 2008; 320: 674-677.
9. Hornung V, Bauernfeind F, Halle A et al. Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat Immunol 2008; 9: 847-856.
10. Dostert C, Guarda G, Romero JF et al. Malarial hemozoin is a Nalp3 inflammasome activating danger signal. PloS One 2009; 4: e6510.
11. Cruz CM, Rinna A, Forman HJ, Ventura AL, Persechini PM, Ojcius DM. ATP activates a reactive oxygen species-dependent oxidative stress response and secretion of proinflammatory cytokines in macrophages. J Biol Chem 2007; 282: 2871-2879.
12. Wen H, Gris D, Lei Y et al. Fatty acid-induced NLRP3-ASC inflammasome activation interferes with insulin signaling. Nat Immunol 2011; 12: 408-415.
13. Zhou R, Tardivel A, Thorens B, Choi I, Tschopp J. Thioredoxin-interacting protein links oxidative stress to inflammasome activation. Nat Immunol 2010; 11: 136-140.
14. Masters SL, Dunne A, Subramanian SL et al. Activation of the NLRP3 inflammasome by islet amyloid polypeptide provides a mechanism for enhanced IL-1beta in type 2 diabetes. Nat Immunol 2010; 10: 897-904.
15. Lee GS, Subramanian N, Kim AI et al. The calcium-sensing receptor regulates the NLRP3 inflammasome through Ca2+ and cAMP. Nature 2012; 492: 123-127.
16. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW Jr. Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 2003; 112: 1796-1808.
17. Hotamisligil GS. Inflammation and metabolic disorders. Nature 2006; 444: 860-867.
18. Feve B, Bastard JP. The role of interleukins in insulin resistance and type 2 diabetes mellitus. Nat Rev Endocrinol 2009; 5: 305-311.
19. Arend WP, Palmer G, Gabay C. IL-1, IL-18, and IL-33 families of cytokines. Immunol Rev 2008; 223: 20-38.
20. Spranger J, Kroke A, Mohlig M et al. Inflammatory cytokines and the risk to develop type 2 diabetes: results of the prospective population-based European Prospective Investigation into Cancer and Nutrition (EPIC)-Potsdam Study. Diabetes 2003; 52: 812-817.
21. Sauter NS, Schulthess FT, Galasso R, Castellani LW, Maedler K. The antiinflammatory cytokine interleukin-1 receptor antagonist protects from high-fat diet-induced hyperglycemia. Endocrinology 2008; 149: 2208-2218.
22. Larsen CM, Faulenbach M, Vaag A et al. Interleukin-1-receptor antagonist in type 2 diabetes mellitus. N Engl J Med 2007; 356: 1517-1526.
23. Jager J, Gremeaux T, Cormont M, Le Marchand-Brustel Y, Tanti JF. Interleukin-1beta-induced insulin resistance in adipocytes through down-regulation of insulin receptor substrate-1 expression. Endocrinology 2007; 148: 241-251.
24. Hotamisligil GS. The role of TNF alpha and TNF receptors in obesity and insulin resistance. J Intern Med 1999; 245: 621-625.
25. Vandanmagsar B, Youm YH, Ravussin A et al. The NLRP3 inflammasome instigates obesity-induced inflammation and insulin resistance. Nat Med 2011; 17: 179-188.
26. Seino S. Study Group of Comprehensive Analysis of Genetic Factors in Diabetes M. S20G mutation of the amylin gene is associated with Type II diabetes in Japanese. Study Group of Comprehensive Analysis of Genetic Factors in Diabetes Mellitus. Diabetologia 2001; 44: 906-909.
27. Oka S, Yoshihara E, Bizen-Abe A et al. Thioredoxin binding protein-2/thioredoxin-interacting protein is a critical regulator of insulin secretion and peroxisome proliferator-activated receptor function. Endocrinology 2009; 150: 1225-1234.
28. Hansson GK. Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med 2005; 352: 1685-1695.
29. Galea J, Armstrong J, Gadsdon P, Holden H, Francis SE, Holt CM. Interleukin-1 beta in coronary arteries of patients with ischemic heart disease. Arterioscler Thromb Vasc Biol 1996; 16: 1000-1006.
30. Moyer CF, Sajuthi D, Tulli H, Williams JK. Synthesis of IL-1 alpha and IL-1 beta by arterial cells in atherosclerosis. Am J Pathol 1991; 138: 951-960.
31. Olofsson PS, Sheikine Y, Jatta K et al. A functional interleukin-1 receptor antagonist polymorphism influences atherosclerosis development. The interleukin-1beta:interleukin-1 receptor antagonist balance in atherosclerosis. Circ J 2009; 73: 1531-1536.
32. Duewell P, Kono H, Rayner KJ et al. NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature 2010; 464: 1357-1361.
33. Freudweiler M. Study of the nature of gouty tophi. Dtsch Arch Klin Med 1899; 63: 36-41.
34. Landis RC, Haskard DO. Pathogenesis of crystal-induced inflammation. Curr Rheumatol Rep 2001; 3: 36-41.
35. Terkeltaub R, Sundy JS, Schumacher HR 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 2009; 68: 1613-1617.
36. McGonagle D, Tan AL, Shankaranarayana S, Madden J, Emery P, McDermott MF. Management of treatment resistant inflammation of acute on chronic tophaceous gout with anakinra. Ann Rheum Dis 2007; 66: 1683-1684.
37. So A, De Smedt T, Revaz S, Tschopp J. A pilot study of IL-1 inhibition by anakinra in acute gout. Arthritis Res Ther 2007; 9: R28.
38. Landis RC, Yagnik DR, Florey O et al. Safe disposal of inflammatory monosodium urate monohydrate crystals by differentiated macrophages. Arthritis Rheum 2002; 46: 3026-3033.
39. Martinon F, Petrilli V, Mayor A, Tardivel A, Tschopp J. Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 2006; 440: 237-241.
40. Joosten LA, Netea MG, Mylona E et al. Engagement of fatty acids with Toll-like receptor 2 drives interleukin-1beta production via the ASC/caspase 1 pathway in monosodium urate monohydrate crystal-induced gouty arthritis. Arthritis Rheum 2010; 62: 3237-3248.
41. Liu-Bryan R, Scott P, Sydlaske A, Rose DM, Terkeltaub R. Innate immunity conferred by Toll-like receptors 2 and 4 and myeloid differentiation factor 88 expression is pivotal to monosodium urate monohydrate crystal-induced inflammation. Arthritis Rheum 2005; 52: 2936-2946.
42. Chen CJ, Shi Y, Hearn A et al. MyD88-dependent IL-1 receptor signaling is essential for gouty inflammation stimulated by monosodium urate crystals. J Clin Invest 2006; 116: 2262-2271.
43. Maedler K, Sergeev P, Ris F et al. Glucose-induced beta cell production of IL-1beta contributes to glucotoxicity in human pancreatic islets. J Clin Invest 2002; 110: 851-860.
44. Shi Y, Evans JE, Rock KL. Molecular identification of a danger signal that alerts the immune system to dying cells. Nature 2003; 425: 516-521.
45. Yoshizaki T, Schenk S, Imamura T et al. SIRT1 inhibits inflammatory pathways in macrophages and modulates insulin sensitivity. Am J Physiol Endocrin Metab 2010; 298: E419-E428.
46. Sag D, Carling D, Stout RD, Suttles J. Adenosine 5'-monophosphate-activated protein kinase promotes macrophage polarization to an anti-inflammatory functional phenotype. J Immunol 2008; 181: 8633-8641.
47. Chalkiadaki A, Guarente L. Sirtuins mediate mammalian metabolic responses to nutrient availability. Nat Rev Endocrinol 2012; 8: 287-296.
48. Picard F, Kurtev M, Chung N, Topark-Ngarm A et al. Sirt1 promotes fat mobilization in white adipocytes by repressing PPAR-gamma. Nature 2004; 429: 771-776.
49. Lin J, Handschin C, Spiegelman BM. Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab 2005; 1: 361-370.
50. Yeung F, Hoberg JE, Ramsey CS et al. Modulation of NF-kappaB-dependent transcription and cell survival by the SIRT1 deacetylase. EMBO J 2004; 23: 2369-2380.
51. Gillum MP, Kotas ME, Erion DM et al. SirT1 regulates adipose tissue inflammation. Diabetes 2011; 60: 3235-3245.
52. Chalkiadaki A, Guarente L. High-fat diet triggers inflammation-induced cleavage of SIRT1 in adipose tissue to promote metabolic dysfunction. Cell Metab 2012; 16: 180-188.
53. Oakhill JS, Steel R, Chen ZP et al. AMPK is a direct adenylate charge-regulated protein kinase. Science 2011; 332: 1433-1435.
54. Jones RG, Plas DR, Kubek S et al. AMP-activated protein kinase induces a p53-dependent metabolic checkpoint. Mol Cell 2005; 18: 283-293.
55. Bolster DR, Crozier SJ, Kimball SR, Jefferson LS. AMP-activated protein kinase suppresses protein synthesis in rat skeletal muscle through down-regulated mammalian target of rapamycin (mTOR) signaling. J Biol Chem 2002; 277: 23977-23980.
56. Sanders MJ, Grondin PO, Hegarty BD, Snowden MA, Carling D. Investigating the mechanism for AMP activation of the AMP-activated protein kinase cascade. Biochem J 2007; 403: 139-148.
57. Towler MC, Hardie DG. AMP-activated protein kinase in metabolic control and insulin signaling. Circ Res 2007; 100: 328-341.
58. Mu J, Barton ER, Birnbaum MJ. Selective suppression of AMP-activated protein kinase in skeletal muscle: update on 'lazy mice'. Biochem Soc Trans 2003; 31: 236-241.
59. Yang Z, Kahn BB, Shi H, Xue BZ. Macrophage alpha1 AMP-activated protein kinase (alpha1AMPK) antagonizes fatty acid-induced inflammation through SIRT1. J Biol Chem 2010; 285: 19051-19059.
60. Pilon G, Dallaire P, Marette A. Inhibition of inducible nitric-oxide synthase by activators of AMP-activated protein kinase: a new mechanism of action of insulin-sensitizing drugs. J Biol Chem 2004; 279: 20767-20774.
61. O'Neill LA, Hardie DG. Metabolism of inflammation limited by AMPK and pseudo-starvation. Nature 2013; 493: 346-355.
62. Hawley SA, Fullerton MD, Ross FA et al. The ancient drug salicylate directly activates AMP-activated protein kinase. Science 2012; 336: 918-922.
63. Yuan M, Konstantopoulos N, Lee J et al. Reversal of obesity- and diet-induced insulin resistance with salicylates or targeted disruption of Ikkbeta. Science 2001; 293: 1673-1677.
64. Goldfine AB, Fonseca V, Jablonski KA et al. The effects of salsalate on glycemic control in patients with type 2 diabetes: a randomized trial. Ann Intern Med 2010; 152: 346-357.
65. Krook A, Wallberg-Henriksson H, Zierath JR. Sending the signal: molecular mechanisms regulating glucose uptake. Med Sci Sports Exerc 2004; 36: 1212-1217.
66. Nakahira K, Haspel JA, Rathinam VA et al. Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat Immunol 2011; 12: 222-230.
67. Krawczyk CM, Holowka T, Sun J et al. Toll-like receptor-induced changes in glycolytic metabolism regulate dendritic cell activation. Blood 2010; 115: 4742-4749.
68. Tannahill GM, Curtis AM, Adamik J. Succinate is a danger signal that induces IL-1β via HIF-1α. Nature 2013; 496: 238-242.
69. Warburg O, Wind F, Negelein E. The metabolism of tumors in the body. J Gen Physiol 1927; 8: 519-530.
70. Rodriguez-Prados JC, Traves PG, Cuenca J et al. Substrate fate in activated macrophages: a comparison between innate, classic, and alternative activation. J Immunol 2010; 185: 605-614.
71. Dang EV, Barbi J, Yang HY et al. Control of T(H)17/T(reg) balance by hypoxia-inducible factor 1. Cell 2011; 146: 772-784.
72. van der Windt GJ, Everts B, Chang CH et al. Mitochondrial respiratory capacity is a critical regulator of CD8+ T cell memory development. Immunity 2012; 36: 68-78.
73. Shao W, Yeretssian G, Doiron K, Hussain SN, Saleh M. The caspase-1 digestome identifies the glycolysis pathway as a target during infection and septic shock. J Biol Chem 2007; 282: 36321-36329.
74. Almeida A, Moncada S, Bolanos JP. Nitric oxide switches on glycolysis through the AMP protein kinase and 6-phosphofructo-2-kinase pathway. Nat Cell Biol 2004; 6: 45-51.
75. Everts B, Amiel E, van der Windt GJ et al. Commitment to glycolysis sustains survival of NO-producing inflammatory dendritic cells. Blood 2012; 120: 1422-1431.