ATP release and purinergic signaling in NLRP3 inflammasome activation

Frontiers in Immunology

Volumn 3, Issue JAN, 2012, Pages

  Gombault, Aurélie ^a   Baron, Ludivine ^a   Couillin, Isabelle ^a  

^a UNIVERSITÉ D'ORLÉANS   (France)

Author keywords

ATP; Autophagic cell death; Danger signal; Inflammasome; NLRP3; P2R; Purinergic signaling

Indexed keywords

EID: 84874280249     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2012.00414     Document Type: Short Survey

References (49)

1. Abbracchio, M. P., Burnstock, G., Boeynaems, J. M., Barnard, E. A., Boyer, J. L., Kennedy, C., et al. (2006). International Union of Pharmacology LVIII: update on the P2Y G protein-coupled nucleotide receptors: from molecular mechanisms and pathophysiol-ogy to therapy. Pharmacol. Rev. 58, 281-341.
2. Aganna, E., Martinon, F., Hawkins, P. N., Ross, J. B., Swan, D. C., Booth, D. R., et al. (2002). Association of mutations in the NALP3/CIAS1/PYPAF1 gene with a broad phenotype including recurrent fever, cold sensitivity, sensorineu-ral deafness, and AA amyloidosis. Arthritis Rheum. 46, 2445-2452.
3. Agostini, L., Martinon, F., Burns, K., Mcdermott, M. F., Hawkins, P. N., and Tschopp, J. (2004). NALP3 forms an IL-1beta-processing inflam-masome with increased activity in Muckle-Wells autoinflammatory disorder. Immunity 20, 319-325.
4. Ataman-Onal, Y., Munier, S., Ganee, A., Terrat, C., Durand, P. Y., Battail, N., et al. (2006). Surfactant-free anionic PLA nanoparticles coated with HIV-1 p24 protein induced enhanced cellular and humoral immune responses in various animal models. J. Control. Release 112, 175-185.
5. Ayna, G., Krysko, D. V., Kaczmarek, A., Petrovski, G., Vandenabeele, P., and Fesus, L. (2012). ATP release from dying autophagic cells and their phagocytosis are crucial for inflammasome activation in macrophages. PLoS ONE 7:e40069. doi: 10.1371/journal.pone.0040069
6. Babelova, A., Moreth, K., Tsalastra-Greul, W., Zeng-Brouwers, J., Eickelberg, O., Young, M. F., et al. (2009). Biglycan, a danger signal that activates the NLRP3 inflammasome via toll-like and P2X receptors. J. Biol. Chem. 284, 24035-24048.
7. Burnstock, G. (2006). Historical review: ATP as a neurotransmitter. Trends Pharmacol. Sci. 27, 166-176.
8. Cassel, S. L., Joly, S., and Sutterwala, F. S. (2009). The NLRP3 inflammasome: a sensor of immune danger signals. Semin. Immunol. 21, 194-198.
9. Codogno, P., and Meijer, A. J. (2005). Autophagy and signaling: their role in cell survival and cell death. Cell Death Differ. 12(Suppl. 2), 1509-1518.
10. Cvetanovic, M., Mitchell, J. E., Patel, V., Avner, B. S., Su, Y., Van Der Saag, P. T., et al. (2006). Specific recognition of apoptotic cells reveals a ubiquitous and unconventional innate immunity. J. Biol. Chem. 281, 20055-20067.
11. De Duve, C., and Wattiaux, R. (1966). Functions of lysosomes. Annu. Rev. Physiol. 28, 435-492.
12. Di Virgilio, F. (2007). Liaisons dan-gereuses: P2X(7) and the inflamma-some. Trends Pharmacol. Sci. 28, 465-472.
13. Di Virgilio, F., Borea, P. A., and Illes, P. (2001). P2 receptors meet the immune system. Trends Pharmacol. Sci. 22, 5-7.
14. Di Virgilio, F., Ferrari, D., Falzoni, S., Chiozzi, P., Munerati, M., Steinberg, T. H., et al. (1996). P2 purinoceptors in the immune system. Ciba Found. Symp. 198, 290-302; discussion 302-305.
15. Dostert, C., Petrilli, V., Van Bruggen, R., Steele, C., Mossman, B. T., and Tschopp, J. (2008). Innate immune activation through Nalp3 inflamma-some sensing of asbestos and silica. Science 320, 674-677.
16. Duewell, P., Kono, H., Rayner, K. J., Sirois, C. M., Vladimer, G., Bauernfeind, F. G., et al. (2010). NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature 464, 1357-1361.
17. Eisenbarth, S. C., Colegio, O. R., O'Connor, W., Sutterwala, F. S., and Flavell, R. A. (2008). Crucial role for the Nalp3 inflammasome in the immunostimulatory properties of aluminium adjuvants. Nature 453, 1122-1126.
18. Fadok, V. A., Bratton, D. L., Konowal, A., Freed, P. W., Westcott, J. Y., and Henson, P. M. (1998). Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-beta, PGE2, and PAF. J. Clin. Invest. 101, 890-898.
19. Ferrari, D., Chiozzi, P., Falzoni, S., Hanau, S., and Di Virgilio, F. (1997). Purinergic modulation of interleukin-1 beta release from microglial cells stimulated with bacterial endotoxin. J. Exp. Med. 185, 579-582.
20. Ferrari, D., Pizzirani, C., Adinolfi, E., Lemoli, R. M., Curti, A., Idzko, M., et al. (2006). The P2X7 receptor: a key player in IL-1 processing and release. J. Immunol. 176, 3877-3883.
21. Ghiringhelli, F., Apetoh, L., Tesniere, A., Aymeric, L., Ma, Y., Ortiz, C., et al. (2009). Activation of the NLRP3 inflammasome in dendritic cells induces IL-1beta-dependent adaptive immunity against tumors. Nat. Med. 15, 1170-1178.
22. Gozuacik, D., and Kimchi, A. (2007). Autophagy and cell death. Curr. Top. Dev. Biol. 78, 217-245.
23. Halle, A., Hornung, V., Petzold, G. C., Stewart, C. R., Monks, B. G., Reinheckel, T., et al. (2008). The NALP3 inflammasome is involved in the innate immune response to amyloid-beta. Nat. Immunol. 9, 857-865.
24. Iyer, S. S., Pulskens, W. P., Sadler, J. J., Butter, L. M., Teske, G. J., Ulland, T. K., et al. (2009). Necrotic cells trigger a sterile inflammatory response through the Nlrp3 inflammasome. Proc. Natl. Acad. Sci. U.S.A. 106, 20388-20393.
25. James, G., and Butt, A. M. (2002). P2Y and P2X purinoceptor mediated Ca2+ signalling in glial cell pathology in the central nervous system. Eur. J. Pharmacol. 447, 247-260.
26. Kanneganti, T. D., Body-Malapel, M., Amer, A., Park, J. H., Whitfield, J., Franchi, L., et al. (2006). Critical role for Cryopyrin/Nalp3 in activation of caspase-1 in response to viral infection and double-stranded RNA. J. Biol. Chem. 281, 36560-36568.
27. Lazarowski, E. R., Boucher, R. C., and Harden, T. K. (2003). Mechanisms of release of nucleotides and integration of their action as P2X- and P2Y-receptor activating molecules. Mol. Pharmacol. 64, 785-795.
28. Maiuri, M. C., Zalckvar, E., Kimchi, A., and Kroemer, G. (2007). Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat. Rev. Mol. Cell Biol. 8, 741-752.
29. Mariathasan, S., Weiss, D. S., Newton, K., Mcbride, J., O'Rourke, K., Roose-Girma, M., et al. (2006). Cryopyrinactivates theinflammasome in response to toxins and ATP. Nature 440, 228-232.
30. Martinon, F., Agostini, L., Meylan, E., and Tschopp, J. (2004). Identification of bacterial muramyl dipeptide as activator of the NALP3/cryopyrin inflammasome. Curr. Biol. 14, 1929-1934.
31. Martinon, F., Mayor, A., and Tschopp, J. (2009). The inflammasomes: guardians of the body. Annu. Rev. Immunol. 27, 229-265.
32. Martinon, F., and Tschopp, J. (2004). Inflammatory caspases: linking an intracellular innate immune system to autoinflammatory diseases. Cell 117, 561-574.
33. McLarnon, J. G., Ryu, J. K., Walker, D. G., and Choi, H. B. (2006). Upregulated expression of puriner-gic P2X(7) receptor in Alzheimer disease and amyloid-beta peptide-treated microglia and in peptide-injected rat hippocampus. J. Neu-ropathol. Exp. Neurol. 65, 1090-1097.
34. Michaud, M., Martins, I., Sukkur-wala, A. Q., Adjemian, S., Ma, Y., Pellegatti, P., et al. (2011). Autophagy-dependent anticancer immune responses induced by chemotherapeutic agents in mice. Science 334, 1573-1577.
35. Netea, M. G., Nold-Petry, C. A., Nold, M. F., Joosten, L. A., Opitz, B., Van Der Meer, J. H., et al. (2009). Differential requirement for the activation of the inflammasome for processing and release of IL-1beta in mono-cytes and macrophages. Blood 113, 2324-2335.
36. Niemi, K., Teirila, L., Lappalainen, J., Rajamaki, K., Baumann, M. H., Oorni, K., et al. (2011). Serum amyloidA activates the NLRP3inflamma-some via P2X7 receptor and a cathep-sin B-sensitive pathway. J. Immunol. 186, 6119-6128.
37. Parvathenani, L. K., Tertyshnikova, S., Greco, C. R., Roberts, S. B., Robertson, B., and Posmantur, R. (2003). P2X7 mediates superoxide production in primary microglia and is up-regulated in a transgenic mouse model of Alzheimer's disease. J. Biol. Chem. 278, 13309-13317.
38. Pelegrin, P., and Surprenant, A. (2007). Pannexin-1 couples to maitotoxin-and nigericin-induced interleukin-1beta release through a dye uptake-independent pathway. J. Biol. Chem. 282, 2386-2394.
39. Perregaux, D., and Gabel, C. A. (1994). 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. 269, 15195-15203.
40. Petrovski, G., Ayna, G., Majai, G., Hodrea, J., Benko, S., Madi, A., et al. (2011). Phagocytosis of cells dying through autophagy induces inflammasome activation and IL-1beta release in human macrophages. Autophagy 7, 321-330.
41. Petrovski, G., Zahuczky, G., Katona, K., Vereb, G., Martinet, W., Nemes, Z., et al. (2007a). Clearance of dying autophagic cells of different origin by professional and non-professional phagocytes. Cell Death Differ. 14, 1117-1128.
42. Petrovski, G., Zahuczky, G., Majai, G., and Fesus, L. (2007b). Phagocytosis of cells dying through autophagy evokes a pro-inflammatory response in macrophages. Autophagy 3, 509-511.
43. Piccini, A., Carta, S., Tassi, S., Lasiglie, D., Fossati, G., and Rubartelli, A. (2008). ATP is released by monocytes stimulated with pathogen-sensing receptor ligands and induces IL-1beta and IL-18 secretion in an autocrine way. Proc. Natl. Acad. Sci. U.S.A. 105, 8067-8072.
44. Praetorius, H. A., and Leipziger, J. (2009). ATP release from non-excitable cells. Purinergic Signal. 5, 433-446.
45. Riteau, N., Baron, L., Villeret, B., Guillou, N., Savigny, F., Ryffel, B., et al. (2012). ATP release and puriner-gic signaling: a common pathway for particle-mediated inflammasome activation. Cell Death Dis. 3, e403.
46. Sanz, J. M., Chiozzi, P., Ferrari, D., Colaianna, M., Idzko, M., Falzoni, S., et al. (2009). Activation of microglia by amyloid {beta} requires P2X7 receptor expression. J. Immunol. 182, 4378-4385.
47. Schroder, K., Zhou, R., and Tschopp, J. (2010). The NLRP3 inflammasome: a sensor for metabolic danger? Science 327, 296-300.
48. Uratsuji, H., Tada, Y., Kawashima, T., Kamata, M., Hau, C. S., Asano, Y., et al. (2012). P2Y6 receptor signaling pathway mediates inflammatory responses induced by monosodium urate crystals. J. Immunol. 188, 436-444.
49. Yegutkin, G. G. (2008). Nucleotide- and nucleoside-converting ectoenzymes: important modulators of purinergic signalling cascade. Biochim. Biophys. Acta 1783, 673-694.