Negative regulation of NLRP3 inflammasome signaling

Protein and Cell

Volumn 4, Issue 4, 2013, Pages 251-258

  Chen, Shuzhen ^a   Sun, Bing ^a,b  

^a INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^b INSTITUTE PASTEUR OF SHANGHAI   (China)

Author keywords

inflammasome; inflammation; negative regulation; NLRP3

Indexed keywords

CARD ONLY PROTEIN; CRYOPYRIN; INFLAMMASOME; INTERFERON; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; MICRORNA; NITRIC OXIDE; PYRIN ONLY PROTEIN; TRIM PROTEIN; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; AUTOPHAGY; CELLULAR IMMUNITY; ENZYME ACTIVATION; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN SECRETION; REVIEW; SIGNAL TRANSDUCTION; STRUCTURE ACTIVITY RELATION; T LYMPHOCYTE; TRANSCRIPTION REGULATION;

EID: 84876439466     PISSN: 1674800X     EISSN: 16748018     Source Type: Journal    
DOI: 10.1007/s13238-013-2128-8     Document Type: Review

References (80)

1. Allen, I. C., Scull, M. A., Moore, C. B., Holl, E. K., McElvania-TeKippe, E., Taxman, D. J., Guthrie, E. H., Pickles, R. J., and Ting, J. P. (2009a). The NLRP3 inflammasome mediates in vivo innate immunity to influenza A virus through recognition of viral RNA. Immunity 30, 556-565.
2. Bartel, D. P. (2009). MicroRNAs: target recognition and regulatory functions. Cell 136, 215-233.
3. Bauernfeind, F., Bartok, E., Rieger, A., Franchi, L., Nunez, G., and Hornung, V. (2011). Cutting edge: reactive oxygen species inhibitors block priming, but not activation, of the NLRP3 inflammasome. J Immunol 187, 613-617.
4. Bauernfeind, F., Rieger, A., Schildberg, F. A., Knolle, P. A., Schmid-Burgk, J. L., and Hornung, V. (2012). NLRP3 Inflammasome Activity Is Negatively Controlled by miR-223. J Immunol 189, 4175-4181.
5. Bogdan, C. (2001). Nitric oxide and the immune response. Nat Immunol 2, 907-916.
6. Bogdan, C., Rollinghoff, M., and Diefenbach, A. (2000). The role of nitric oxide in innate immunity. Immunol Rev 173, 17-26.
7. Burckstummer, T., Baumann, C., Bluml, S., Dixit, E., Durnberger, G., Jahn, H., Planyavsky, M., Bilban, M., Colinge, J., Bennett, K. L., et al. (2009). An orthogonal proteomic-genomic screen identifies AIM2 as a cytoplasmic DNA sensor for the inflammasome. Nat Immunol 10, 266-272.
8. Chae, J. J., Cho, Y. H., Lee, G. S., Cheng, J., Liu, P. P., Feigenbaum, L., Katz, S. I., and Kastner, D. L. (2011). Gain-of-function Pyrin mutations induce NLRP3 protein-independent interleukin-1beta activation and severe autoinflammation in mice. Immunity 34, 755-768.
9. Chae, J. J., Komarow, H. D., Cheng, J., Wood, G., Raben, N., Liu, P. P., and Kastner, D. L. (2003). Targeted disruption of pyrin, the FMF protein, causes heightened sensitivity to endotoxin and a defect in macrophage apoptosis. Mol Cell 11, 591-604.
10. Clancy, R. M., Amin, A. R., and Abramson, S. B. (1998). The role of nitric oxide in inflammation and immunity. Arthritis Rheum 41, 1141-1151.
11. De Nardo, D., and Latz, E. (2011). NLRP3 inflammasomes link inflammation and metabolic disease. Trends Immunol 32, 373-379.
12. Denoble, A. E., Huffman, K. M., Stabler, T. V., Kelly, S. J., Hershfield, M. S., McDaniel, G. E., Coleman, R. E., and Kraus, V. B. (2011). Uric acid is a danger signal of increasing risk for osteoarthritis through inflammasome activation. Proc Natl Acad Sci U S A 108, 2088-2093.
13. Dorfleutner, A., Bryan, N. B., Talbott, S. J., Funya, K. N., Rellick, S. L., Reed, J. C., Shi, X., Rojanasakul, Y., Flynn, D. C., and Stehlik, C. (2007). Cellular pyrin domain-only protein 2 is a candidate regulator of inflammasome activation. Infect Immun 75, 1484-1492.
14. Dostert, C., Petrilli, V., van Bruggen, R., Steele, C., Mossman, B. T., and Tschopp, J. (2008). Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science 320, 674-677.
15. Druilhe, A., Srinivasula, S. M., Razmara, M., Ahmad, M., and Alnemri, E. S. (2001). Regulation of IL-1beta generation by Pseudo-ICE and ICEBERG, two dominant negative caspase recruitment domain proteins. Cell Death Differ 8, 649-657.
16. Duewell, P., Kono, H., Rayner, K. J., Sirois, C. M., Vladimer, G., Bauernfeind, F. G., Abela, G. S., Franchi, L., Nunez, G., Schnurr, M., 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. Fernandes-Alnemri, T., Yu, J. W., Datta, P., Wu, J., and Alnemri, E. S. (2009). AIM2 activates the inflammasome and cell death in response to cytoplasmic DNA. Nature 458, 509-513.
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. Franchi, L., Amer, A., Body-Malapel, M., Kanneganti, T. D., Ozoren, N., Jagirdar, R., Inohara, N., Vandenabeele, P., Bertin, J., Coyle, A., et al. (2006). Cytosolic flagellin requires Ipaf for activation of caspase-1 and interleukin 1beta in salmonella-infected macrophages. Nat Immunol 7, 576-582.
21. Gong, Y. N., and Shao, F. (2012). Sensing bacterial infections by NAIP receptors in NLRC4 inflammasome activation. Protein Cell 3, 98-105.
22. Gram, A. M., Frenkel, J., and Ressing, M. E. (2012). Inflammasomes and viruses: cellular defence versus viral offence. J Gen Virol 93, 2063-2075.
23. Gregory, S. M., Davis, B. K., West, J. A., Taxman, D. J., Matsuzawa, S., Reed, J. C., Ting, J. P., and Damania, B. (2011). Discovery of a viral NLR homolog that inhibits the inflammasome. Science 331, 330-334.
24. Gross, O., Poeck, H., Bscheider, M., Dostert, C., Hannesschlager, N., Endres, S., Hartmann, G., Tardivel, A., Schweighoffer, E., Tybulewicz, V., et al. (2009). Syk kinase signalling couples to the Nlrp3 inflammasome for anti-fungal host defence. Nature 459, 433-436.
25. Gross, O., Thomas, C. J., Guarda, G., and Tschopp, J. (2011). The in-flammasome: an integrated view. Immunol Rev 243, 136-151.
26. Guarda, G., Braun, M., Staehli, F., Tardivel, A., Mattmann, C., Forster, I., Farlik, M., Decker, T., Du Pasquier, R. A., Romero, P., et al. (2011). Type I interferon inhibits interleukin-1 production and inflammasome activation. Immunity 34, 213-223.
27. Guarda, G., Dostert, C., Staehli, F., Cabalzar, K., Castillo, R., Tardivel, A., Schneider, P., and Tschopp, J. (2009). T cells dampen innate immune responses through inhibition of NLRP1 and NLRP3 inflammasomes. Nature 460, 269-273.
28. Halle, A., Hornung, V., Petzold, G. C., Stewart, C. R., Monks, B. G., Reinheckel, T., Fitzgerald, K. A., Latz, E., Moore, K. J., and Golenbock, D. T. (2008). The NALP3 inflammasome is involved in the innate immune response to amyloid-beta. Nat Immunol 9, 857-865.
29. Haneklaus, M., Gerlic, M., Kurowska-Stolarska, M., Rainey, A. A., Pich, D., McInnes, I. B., Hammerschmidt, W., O'Neill, L. A., and Masters, S. L. (2012). Cutting Edge: miR-223 and EBV miR-BART15 Regulate the NLRP3 Inflammasome and IL-1beta Production. J Immunol 189, 3795-3799.
30. Harris, J., Hartman, M., Roche, C., Zeng, S. G., O'Shea, A., Sharp, F. A., Lambe, E. M., Creagh, E. M., Golenbock, D. T., Tschopp, J., et al. (2011). Autophagy controls IL-1beta secretion by targeting pro-IL-1beta for degradation. J Biol Chem 286, 9587-9597.
31. Hernandez-Cuellar, E., Tsuchiya, K., Hara, H., Fang, R., Sakai, S., Kawamura, I., Akira, S., and Mitsuyama, M. (2012). Cutting Edge: Nitric Oxide Inhibits the NLRP3 Inflammasome. The Journal of Immunology 189, 5113-5117.
32. Hoffman, H. M., Rosengren, S., Boyle, D. L., Cho, J. Y., Nayar, J., Mueller, J. L., Anderson, J. P., Wanderer, A. A., and Firestein, G. S. (2004). Prevention of cold-associated acute inflammation in familial cold autoinflammatory syndrome by interleukin-1 receptor antagonist. Lancet 364, 1779-1785.
33. Hornung, V., Ablasser, A., Charrel-Dennis, M., Bauernfeind, F., Horvath, G., Caffrey, D. R., Latz, E., and Fitzgerald, K. A. (2009). AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating in-flammasome with ASC. Nature 458, 514-518.
34. Hornung, V., Bauernfeind, F., Halle, A., Samstad, E. O., Kono, H., Rock, K. L., Fitzgerald, K. A., and Latz, E. (2008). Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat Immunol 9, 847-856.
35. Hu, Y., Mao, K., Zeng, Y., Chen, S., Tao, Z., Yang, C., Sun, S., Wu, X., Meng, G., and Sun, B. (2010). Tripartite-motif protein 30 negatively regulates NLRP3 inflammasome activation by modulating reactive oxygen species production. J Immunol 185, 7699-7705.
36. Humke, E. W., Shriver, S. K., Starovasnik, M. A., Fairbrother, W. J., and Dixit, V. M. (2000). ICEBERG: a novel inhibitor of interleukin-1beta generation. Cell 103, 99-111.
37. Ichinohe, T., Lee, H. K., Ogura, Y., Flavell, R., and Iwasaki, A. (2009). Inflammasome recognition of influenza virus is essential for adaptive immune responses. J Exp Med 206, 79-87.
38. Johnston, J. B., Barrett, J. W., Nazarian, S. H., Goodwin, M., Ricciuto, D., Wang, G., and McFadden, G. (2005). A poxvirus-encoded pyrin domain protein interacts with ASC-1 to inhibit host inflammatory and apoptotic responses to infection. Immunity 23, 587-598.
39. Kahlenberg, J. M., and Dubyak, G. R. (2004). Differing caspase-1 activation states in monocyte versus macrophage models of IL-1beta processing and release. J Leukoc Biol 76, 676-684.
40. Komune, N., Ichinohe, T., Ito, M., and Yanagi, Y. (2011). Measles virus V protein inhibits NLRP3 inflammasome-mediated interleukin-1beta secretion. J Virol 85, 13019-13026.
41. Kumar, H., Kumagai, Y., Tsuchida, T., Koenig, P. A., Satoh, T., Guo, Z., Jang, M. H., Saitoh, T., Akira, S., and Kawai, T. (2009). Involvement of the NLRP3 inflammasome in innate and humoral adaptive immune responses to fungal beta-glucan. J Immunol 183, 8061-8067.
42. Lamkanfi, M. (2011). Emerging inflammasome effector mechanisms. Nat Rev Immunol 11, 213-220.
43. Lamkanfi, M., Denecker, G., Kalai, M., D'Hondt, K., Meeus, A., Declercq, W., Saelens, X., and Vandenabeele, P. (2004). INCA, a novel human caspase recruitment domain protein that inhibits interleukin-1beta generation. J Biol Chem 279, 51729-51738.
44. Lamkanfi, M., and Dixit, V. M. (2009). Inflammasomes: guardians of cytosolic sanctity. Immunol Rev 227, 95-105.
45. Levine, B., Mizushima, N., and Virgin, H. W. (2011). Autophagy in immunity and inflammation. Nature 469, 323-335.
46. Mao, K., Chen, S., Chen, M., Ma, Y., Wang, Y., Huang, B., He, Z., Zeng, Y., Hu, Y., Sun, S., et al. (2013). Nitric oxide suppresses NLRP3 inflammasome activation and protects against LPS-induced septic shock. Cell Research 23, 201-212.
47. Mariathasan, S., Weiss, D. S., Newton, K., McBride, J., O'Rourke, K., Roose-Girma, M., Lee, W. P., Weinrauch, Y., Monack, D. M., and Dixit, V. M. (2006). Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 440, 228-232.
48. Martinon, F., Burns, K., and Tschopp, J. (2002). The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol Cell 10, 417-426.
49. Martinon, F., Mayor, A., and Tschopp, J. (2009). The inflammasomes: guardians of the body. Annu Rev Immunol 27, 229-265.
50. Martinon, F., Petrilli, V., Mayor, A., Tardivel, A., and Tschopp, J. (2006). Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 440, 237-241.
51. Martinon, F., and Tschopp, J. (2004). Inflammatory caspases: linking an intracellular innate immune system to autoinflammatory diseases. Cell 117, 561-574.
52. Masters, S. L., Dunne, A., Subramanian, S. L., Hull, R. L., Tannahill, G. M., Sharp, F. A., Becker, C., Franchi, L., Yoshihara, E., Chen, Z., et al. (2010). Activation of the NLRP3 inflammasome by islet amyloid polypeptide provides a mechanism for enhanced IL-1beta in type 2 diabetes. Nat Immunol 11, 897-904.
53. Mayer-Barber, K. D., Andrade, B. B., Barber, D. L., Hieny, S., Feng, C. G., Caspar, P., Oland, S., Gordon, S., and Sher, A. (2011). Innate and adaptive interferons suppress IL-1alpha and IL-1beta production by distinct pulmonary myeloid subsets during Mycobacterium tuberculosis infection. Immunity 35, 1023-1034.
54. Meixenberger, K., Pache, F., Eitel, J., Schmeck, B., Hippenstiel, S., Slevogt, H., N'Guessan, P., Witzenrath, M., Netea, M. G., Chakraborty, T., et al. (2010). Listeria monocytogenes-infected human peripheral blood mononuclear cells produce IL-1beta, depending on listeriolysin O and NLRP3. J Immunol 184, 922-930.
55. Miao, E. A., Alpuche-Aranda, C. M., Dors, M., Clark, A. E., Bader, M. W., Miller, S. I., and Aderem, A. (2006). Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1beta via Ipaf. Nat Immunol 7, 569-575.
56. Mishra, B. B., Rathinam, V. A., Martens, G. W., Martinot, A. J., Kornfeld, H., Fitzgerald, K. A., and Sassetti, C. M. (2012). Nitric oxide controls the immunopathology of tuberculosis by inhibiting NLRP3 inflammasome-dependent processing of IL-1beta. Nat Immunol 14, 52-60.
57. Munoz-Planillo, R., Franchi, L., Miller, L. S., and Nunez, G. (2009). A critical role for hemolysins and bacterial lipoproteins in Staphylococcus aureus-induced activation of the Nlrp3 inflammasome. J Immunol 183, 3942-3948.
58. Nakahira, K., Haspel, J. A., Rathinam, V. A., Lee, S. J., Dolinay, T., Lam, H. C., Englert, J. A., Rabinovitch, M., Cernadas, M., Kim, H. P., et al. (2011). Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat Immunol 12, 222-230.
59. Netea, M. G., Nold-Petry, C. A., Nold, M. F., Joosten, L. A., Opitz, B., van der Meer, J. H., van de Veerdonk, F. L., Ferwerda, G., Heinhuis, B., Devesa, I., et al. (2009). Differential requirement for the activation of the inflammasome for processing and release of IL-1beta in monocytes and macrophages. Blood 113, 2324-2335.
60. Niedbala, W., Alves-Filho, J. C., Fukada, S. Y., Vieira, S. M., Mitani, A., Sonego, F., Mirchandani, A., Nascimento, D. C., Cunha, F. Q., and Liew, F. Y. (2011). Regulation of type 17 helper T-cell function by nitric oxide during inflammation. Proc Natl Acad Sci U S A 108, 9220-9225.
61. Rawlingson, A. (2003). Nitric oxide, inflammation and acute burn injury. Burns 29, 631-640.
62. Roberts, T. L., Idris, A., Dunn, J. A., Kelly, G. M., Burnton, C. M., Hodgson, S., Hardy, L. L., Garceau, V., Sweet, M. J., Ross, I. L., et al. (2009). HIN-200 proteins regulate caspase activation in response to foreign cytoplasmic DNA. Science 323, 1057-1060.
63. Rosengren, S., Mueller, J. L., Anderson, J. P., Niehaus, B. L., Misaghi, A., Anderson, S., Boyle, D. L., and Hoffman, H. M. (2007). Monocytes from familial cold autoinflammatory syndrome patients are activated by mild hypothermia. J Allergy Clin Immunol 119, 991-996.
64. Rosenstiel, P., Huse, K., Till, A., Hampe, J., Hellmig, S., Sina, C., Billmann, S., von Kampen, O., Waetzig, G. H., Platzer, M., et al. (2006). A short isoform of NOD2/CARD15, NOD2-S, is an endogenous inhibitor of NOD2/receptor-interacting protein kinase 2-induced signaling pathways. Proc Natl Acad Sci U S A 103, 3280-3285.
65. Saitoh, T., Fujita, N., Jang, M. H., Uematsu, S., Yang, B. G., Satoh, T., Omori, H., Noda, T., Yamamoto, N., Komatsu, M., et al. (2008). Loss of the autophagy protein Atg16L1 enhances endotoxininduced IL-1beta production. Nature 456, 264-268.
66. Saleh, M., Mathison, J. C., Wolinski, M. K., Bensinger, S. J., Fitzgerald, P., Droin, N., Ulevitch, R. J., Green, D. R., and Nicholson, D. W. (2006). Enhanced bacterial clearance and sepsis resistance in caspase-12-deficient mice. Nature 440, 1064-1068.
67. Saleh, M., Vaillancourt, J. P., Graham, R. K., Huyck, M., Srinivasula, S. M., Alnemri, E. S., Steinberg, M. H., Nolan, V., Baldwin, C. T., Hotchkiss, R. S., et al. (2004). Differential modulation of endotoxin responsiveness by human caspase-12 polymorphisms. Nature 429, 75-79.
68. Schroder, K., and Tschopp, J. (2010). The inflammasomes. Cell 140, 821-832.
69. Shi, C. S., Shenderov, K., Huang, N. N., Kabat, J., Abu-Asab, M., Fitzgerald, K. A., Sher, A., and Kehrl, J. H. (2012). Activation of autophagy by inflammatory signals limits IL-1beta production by targeting ubiquitinated inflammasomes for destruction. Nat Immunol 13, 255-263.
70. Shimada, K., Crother, T. R., Karlin, J., Dagvadorj, J., Chiba, N., Chen, S., Ramanujan, V. K., Wolf, A. J., Vergnes, L., Ojcius, D. M., et al. (2012). Oxidized mitochondrial DNA activates the NLRP3 inflammasome during apoptosis. Immunity 36, 401-414.
71. Shio, M. T., Eisenbarth, S. C., Savaria, M., Vinet, A. F., Bellemare, M. J., Harder, K. W., Sutterwala, F. S., Bohle, D. S., Descoteaux, A., Flavell, R. A., et al. (2009). Malarial hemozoin activates the NLRP3 inflammasome through Lyn and Syk kinases. PLoS Pathog 5, e1000559.
72. Stehlik, C., and Dorfleutner, A. (2007). COPs and POPs: modulators of inflammasome activity. J Immunol 179, 7993-7998.
73. Strowig, T., Henao-Mejia, J., Elinav, E., and Flavell, R. (2012). Inflammasomes in health and disease. Nature 481, 278-286.
74. Sutterwala, F. S., Ogura, Y., Szczepanik, M., Lara-Tejero, M., Lichtenberger, G. S., Grant, E. P., Bertin, J., Coyle, A. J., Galan, J. E., Askenase, P. W., et al. (2006). Critical role for NALP3/CIAS1/Cryopyrin in innate and adaptive immunity through its regulation of caspase-1. Immunity 24, 317-327.
75. Takeuchi, O., and Akira, S. (2010). Pattern recognition receptors and inflammation. Cell 140, 805-820.
76. Tschopp, J., and Schroder, K. (2010). NLRP3 inflammasome activation: The convergence of multiple signalling pathways on ROS production? Nat Rev Immunol 10, 210-215.
77. Wen, H., Gris, D., Lei, Y., Jha, S., Zhang, L., Huang, M. T., Brickey, W. J., and Ting, J. P. (2011). Fatty acid-induced NLRP3-ASC inflammasome activation interferes with insulin signaling. Nat Immunol 12, 408-415.
78. Zhao, Y., Yang, J., Shi, J., Gong, Y. N., Lu, Q., Xu, H., Liu, L., and Shao, F. (2011). The NLRC4 inflammasome receptors for bacterial flagellin and type III secretion apparatus. Nature 477, 596-600.
79. Zhou, R., Tardivel, A., Thorens, B., Choi, I., and Tschopp, J. (2010). Thioredoxin-interacting protein links oxidative stress to inflammasome activation. Nat Immunol 11, 136-140.
80. Zhou, R., Yazdi, A. S., Menu, P., and Tschopp, J. (2011). A role for mitochondria in NLRP3 inflammasome activation. Nature 469, 221-225.