Xanthine oxidoreductase regulates macrophage IL1β secretion upon NLRP3 inflammasome activation

Nature Communications

Volumn 6, Issue , 2015, Pages

  Ives, Annette ^a   Nomura, Johji ^a,b   Martinon, Fabio ^c   Roger, Thierry ^a   LeRoy, Didier ^a   Miner, Jeffrey N ^d   Simon, Gregoire ^a   Busso, Nathalie ^a   So, Alexander ^a  

^a LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^b TEIJIN LTD   (Japan)

^c UNIVERSITY OF LAUSANNE   (Switzerland)

^d Ardea Biosciences Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; ADENOSINE TRIPHOSPHATE; ALLOPURINOL; APOCYNIN; CASPASE; CRYOPYRIN; FEBUXOSTAT; INFLAMMASOME; INTERLEUKIN 1BETA; MAMMALIAN TARGET OF RAPAMYCIN; PHORBOL 13 ACETATE 12 MYRISTATE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; RAPAMYCIN; RASBURICASE; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA; URIC ACID; WORTMANNIN; XANTHINE OXIDASE; CALCIUM; CALCIUM PHOSPHATE; CARRIER PROTEIN; INTERLEUKIN 1BETA CONVERTING ENZYME; LIPOPOLYSACCHARIDE; NLRP3 PROTEIN, HUMAN; NLRP3 PROTEIN, MOUSE; XANTHINE DEHYDROGENASE;

CYTOPLASM; ENZYME ACTIVITY; IMMUNE SYSTEM; LIGAND; MITOCHONDRIAL DNA; OXIDATION; SECRETION; SIGNALING;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL FRACTIONATION; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME REGULATION; FEMALE; HUMAN; HUMAN CELL; INFLAMMATORY DISEASE; MACROPHAGE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; MONOCYTE; MOUSE; NONHUMAN; PROTEIN PHOSPHORYLATION; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; AUTOPHAGY; C57BL MOUSE; DRUG EFFECTS; GENE SILENCING; GENETICS; IMMUNOLOGY; IN VITRO STUDY; METABOLISM; PERITONITIS; PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SECRETION (PROCESS); SIGNAL TRANSDUCTION;

ANIMALS; AUTOPHAGY; BLOTTING, WESTERN; CALCIUM; CALCIUM PHOSPHATES; CARRIER PROTEINS; CASPASE 1; GENE KNOCKDOWN TECHNIQUES; IN VITRO TECHNIQUES; INTERLEUKIN-1BETA; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; MICE, INBRED C57BL; MONOCYTES; NLR FAMILY, PYRIN DOMAIN-CONTAINING 3 PROTEIN; PERITONITIS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; REACTIVE OXYGEN SPECIES; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; URIC ACID; XANTHINE DEHYDROGENASE; XANTHINE OXIDASE;

EID: 84925353327     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms7555     Document Type: Article

References (55)

1. Gross, O., Thomas, C. J., Guarda, G. & Tschopp, J. The inflammasome: an integrated view. Immunol. Rev. 243, 136-151 (2011).
2. Subramanian, N., Natarajan, K., Clatworthy, M. R., Wang, Z. & Germain, R. N. The adaptor MAVS promotes NLRP3 mitochondrial localization and inflammasome activation. Cell 153, 348-361 (2013).
3. Hornung, V. et al. Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat. Immunol. 9, 847-856 (2008).
4. Lu, B. et al. Novel role of PKR in inflammasome activation and HMGB1 release. Nature 488, 670-674 (2012).
5. Petrilli, V. et al. Activation of the NALP3 inflammasome is triggered by low intracellular potassium concentration. Cell Death Differ. 14, 1583-1589 (2007).
6. Lee, G. S. et al. The calcium-sensing receptor regulates the NLRP3 inflammasome through Ca(2+) and cAMP. Nature 492, 123-127 (2012).
7. Dostert, C. et al. Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science 320, 674-677 (2008).
8. Cassel, S. L. et al. The Nalp3 inflammasome is essential for the development of silicosis. Proc. Natl Acad. Sci. USA 105, 9035-9040 (2008).
9. Meissner, F. et al. Inflammasome activation in NADPH oxidase defective mononuclear phagocytes from patients with chronic granulomatous disease. Blood 116, 1570-1573 (2010).
10. Zhou, R., Yazdi, A. S., Menu, P. & Tschopp, J. A role for mitochondria in NLRP3 inflammasome activation. Nature 469, 221-225 (2011).
11. 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).
12. Nomura, J. et al. Febuxostat, an inhibitor of xanthine oxidase, suppresses lipopolysaccharide-induced MCP-1 production via MAPK phosphatase-1-mediated inactivation of JNK. PLoS ONE 8, e75527 (2013).
13. George, J. & Struthers, A. D. Role of urate, xanthine oxidase and the effects of allopurinol in vascular oxidative stress. Vasc. Health Risk Manag. 5, 265-272 (2009).
14. Feig, D. I., Soletsky, B. & Johnson, R. J. Effect of allopurinol on blood pressure of adolescents with newly diagnosed essential hypertension: a randomized trial. JAMA 300, 924-932 (2008).
15. Kao, M. P. et al. Allopurinol benefits left ventricular mass and endothelial dysfunction in chronic kidney disease. J. Am. Soc. Nephrol. 22, 1382-1389 (2011).
16. So, A. & Thorens, B. Uric acid transport and disease. J. Clin. Invest. 120, 1791-1799 (2010).
17. Shi, Y., Evans, J. E. & Rock, K. L. Molecular identification of a danger signal that alerts the immune system to dying cells. Nature 425, 516-521 (2003).
18. Kono, H., Chen, C. J., Ontiveros, F. & Rock, K. L. Uric acid promotes an acute inflammatory response to sterile cell death in mice. J. Clin. Invest. 120, 1939-1949 (2010).
19. Orengo, J. M. et al. Uric acid is a mediator of the Plasmodium falciparum-induced inflammatory response. PLoS ONE 4, e5194 (2009).
20. 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).
21. Nicholas, S. A., Bubnov, V. V., Yasinska, I. M. & Sumbayev, V. V. Involvement of xanthine oxidase and hypoxia-inducible factor 1 in Toll-like receptor 7/8-mediated activation of caspase 1 and interleukin-1beta. Cell. Mol. Life Sci. 68, 151-158 (2011).
22. Griffith, J. W., Sun, T., McIntosh, M. T. & Bucala, R. Pure Hemozoin is inflammatory in vivo and activates the NALP3 inflammasome via release of uric acid. J. Immunol. 183, 5208-5220 (2009).
23. Jin, C. et al. NLRP3 inflammasome plays a critical role in the pathogenesis of hydroxyapatite-associated arthropathy. Proc. Natl Acad. Sci. USA 108, 14867-14872 (2011).
24. Kool, M. et al. Cutting edge: alum adjuvant stimulates inflammatory dendritic cells through activation of the NALP3 inflammasome. J. Immunol. 181, 3755-3759 (2008).
25. Pazar, B. et al. Basic calcium phosphate crystals induce monocyte/macrophage IL-1beta secretion through the NLRP3 inflammasome in vitro. J. Immunol. 186, 2495-2502 (2011).
26. Takano, Y. et al. Selectivity of febuxostat, a novel non-purine inhibitor of xanthine oxidase/xanthine dehydrogenase. Life Sci. 76, 1835-1847 (2005).
27. Klinenberg, J. R., Goldfinger, S. E. & Seegmiller, J. E. The effectiveness of the xanthine oxidase inhibitor allopurinol in the treatment of gout. Ann. Intern. Med. 62, 639-647 (1965).
28. Duewell, P. et al. NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature 464, 1357-1361 (2010).
29. Beckman, J. S., Parks, D. A., Pearson, J. D., Marshall, P. A. & Freeman, B. A. A sensitive fluorometric assay for measuring xanthine dehydrogenase and oxidase in tissues. Free Radic. Biol. Med. 6, 607-615 (1989).
30. Cruz, C. M. et al. ATP activates a reactive oxygen species-dependent oxidative stress response and secretion of proinflammatory cytokines in macrophages. J. Biol. Chem. 282, 2871-2879 (2007).
31. Cunningham, C. C. et al. Osteoarthritis-associated basic calcium phosphate crystals induce pro-inflammatory cytokines and damage-associated molecules via activation of Syk and PI3 kinase. Clin. Immunol. 144, 228-236 (2012).
32. Shio, M. T. et al. Malarial hemozoin activates the NLRP3 inflammasome through Lyn and Syk kinases. PLoS Pathog. 5, e1000559 (2009).
33. Harris, J. et al. Autophagy controls IL-1{beta} secretion by targeting pro-IL-1{beta} for degradation. J. Biol. Chem. 286, 9587-9597 (2011).
34. Saitoh, T. et al. Loss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1beta production. Nature 456, 264-268 (2008).
35. Pelletier, M., Lepow, T. S., Billingham, L. K., Murphy, M. P. & Siegel, R. M. New tricks from an old dog: mitochondrial redox signaling in cellular inflammation. Semin. Immunol. 24, 384-392 (2012).
36. Latz, E., Xiao, T. S. & Stutz, A. Activation and regulation of the inflammasomes. Nat. Rev. Immunol. 13, 397-411 (2013).
37. Murphy, M. P. How mitochondria produce reactive oxygen species. Biochem. J. 417, 1-13 (2009).
38. Nishino, T. et al. Mechanism of the conversion of xanthine dehydrogenase to xanthine oxidase: identification of the two cysteine disulfide bonds and crystal structure of a non-convertible rat liver xanthine dehydrogenase mutant. J. Biol. Chem. 280, 24888-24894 (2005).
39. Amaya, Y. et al. Proteolytic conversion of xanthine dehydrogenase from the NAD-dependent type to the O2-dependent type. Amino acid sequence of rat liver xanthine dehydrogenase and identification of the cleavage sites of the enzyme protein during irreversible conversion by trypsin. J. Biol. Chem. 265, 14170-14175 (1990).
40. Enroth, C. et al. Crystal structures of bovine milk xanthine dehydrogenase and xanthine oxidase: structure-based mechanism of conversion. Proc. Natl Acad. Sci. USA 97, 10723-10728 (2000).
41. Ohtsubo, T., Rovira, I. I., Starost, M. F., Liu, C. & Finkel, T. Xanthine oxidoreductase is an endogenous regulator of cyclooxygenase-2. Circ. Res. 95, 1118-1124 (2004).
42. Vorbach, C., Scriven, A. & Capecchi, M. R. The housekeeping gene xanthine oxidoreductase is necessary for milk fat droplet enveloping and secretion: gene sharing in the lactating mammary gland. Genes Dev. 16, 3223-3235 (2002).
43. Carracedo, A. & Pandolfi, P. P. The PTEN-PI3K pathway: of feedbacks and cross-talks. Oncogene 27, 5527-5541 (2008).
44. Leslie, N. R. et al. Redox regulation of PI 3-kinase signalling via inactivation of PTEN. EMBO J. 22, 5501-5510 (2003).
45. Shi, C. S. et al. Activation of autophagy by inflammatory signals limits IL-1beta production by targeting ubiquitinated inflammasomes for destruction. Nat. Immunol. 13, 255-263 (2012).
46. Harris, J. et al. Autophagy controls IL-1beta secretion by targeting pro-IL-1beta for degradation. J. Biol. Chem. 286, 9587-9597 (2011).
47. Degtyarev, M. et al. Akt inhibition promotes autophagy and sensitizes PTEN-null tumors to lysosomotropic agents. J. Cell. Biol. 183, 101-116 (2008).
48. Feig, D. I., Kang, D. H. & Johnson, R. J. Uric acid and cardiovascular risk. N. Engl. J. Med. 359, 1811-1821 (2008).
49. Feig, D. I., Madero, M., Jalal, D. I., Sanchez-Lozada, L. G. & Johnson, R. J. Uric acid and the origins of hypertension. J. Pediatr. 162, 896-902 (2013).
50. Sanchez-Lozada, L. G. et al. Treatment with the xanthine oxidase inhibitor febuxostat lowers uric acid and alleviates systemic and glomerular hypertension in experimental hyperuricaemia. Nephrol. Dial. Transplant 23, 1179-1185 (2008).
51. Muir, S. W. et al. Allopurinol use yields potentially beneficial effects on inflammatory indices in those with recent ischemic stroke: a randomized, double-blind, placebo-controlled trial. Stroke 39, 3303-3307 (2008).
52. Soletsky, B. & Feig, D. I. Uric acid reduction rectifies prehypertension in obese adolescents. Hypertension 60, 1148-1156 (2012).
53. Kushiyama, A. et al. Xanthine oxidoreductase is involved in macrophage foam cell formation and atherosclerosis development. Arterioscler. Thromb. Vasc. Biol. 32, 291-298 (2012).
54. Narayan, S. et al. Octacalcium phosphate crystals induce inflammation in vivo through interleukin-1 but independent of the NLRP3 inflammasome in mice. Arthritis Rheum. 63, 422-433 (2011).
55. Akhtar, N. & Haqqi, T. M. Epigallocatechin-3-gallate suppresses the global interleukin-1beta-induced inflammatory response in human chondrocytes. Arthritis Res. Ther. 13, R93 (2011).