Lipopolysaccharide primes the NALP3 inflammasome by inhibiting its ubiquitination and degradation mediated by the SCFFBXL2 E3 ligase

Journal of Biological Chemistry

Volumn 290, Issue 29, 2015, Pages 18124-18133

  Han, Seung Hye ^a   Lear, Travis B ^a   Jerome, Jacob A ^a   Rajbhandari, Shristi ^a   Snavely, Courtney A ^a   Gulick, Dexter L ^a   Gibson, Kevin F ^a   Zou, Chunbin ^a   Chen, Bill B ^a   Mallampalli, Rama K ^a,b,c  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMICAL ACTIVATION; CYTOLOGY; PROTEINS;

INFLAMMATORY CELLS; LIPOPOLYSACCHARIDES; MOLECULAR TARGETS; MULTI-PROTEIN COMPLEX; NALP3 INFLAMMASOME; PRO-INFLAMMATORY CYTOKINES; PROINFLAMMATORY RESPONSE; SMALL MOLECULE INHIBITOR;

CELLS;

CRYOPYRIN; F BOX L2 PROTEIN; F BOX O3 PROTEIN; F BOX PROTEIN; INTERLEUKIN 18; INTERLEUKIN 1BETA; LIPOPOLYSACCHARIDE; MESSENGER RNA; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; CARRIER PROTEIN; FBX3 PROTEIN, HUMAN; FBXL2 PROTEIN, HUMAN; INFLAMMASOME; NLRP3 PROTEIN, HUMAN; UBIQUITIN PROTEIN LIGASE;

ARTICLE; CONTROLLED STUDY; CRYOPYRIN GENE; CYTOKINE RELEASE; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; INFLAMMATORY CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; STEADY STATE; UBIQUITINATION; CELL LINE; IMMUNOLOGY; INNATE IMMUNITY; METABOLISM;

CARRIER PROTEINS; CELL LINE; F-BOX PROTEINS; HUMANS; IMMUNITY, INNATE; INFLAMMASOMES; INTERLEUKIN-18; INTERLEUKIN-1BETA; LIPOPOLYSACCHARIDES; PROTEOLYSIS; SKP CULLIN F-BOX PROTEIN LIGASES; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84937468257     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.645549     Document Type: Article

References (25)

1. Franchi, L., Muñoz-Planillo, R., and Núñez, G. (2012) Sensing and reacting to microbes through the inflammasomes. Nat. Immunol. 13, 325-332
2. Makabe, H., Kojika, M., Takahashi, G., Matsumoto, N., Shibata, S., Suzuki, Y., Inoue, Y., and Endo, S. (2012) Interleukin-18 levels reflect the longterm prognosis of acute lung injury and acute respiratory distress syndrome. J. Anesth. 26, 658-663
3. Dolinay, T., Kim, Y. S., Howrylak, J., Hunninghake, G. M., An, C. H., Fredenburgh, L., Massaro, A. F., Rogers, A., Gazourian, L., Nakahira, K., Haspel, J. A., Landazury, R., Eppanapally, S., Christie, J. D., Meyer, N. J., Ware, L. B., Christiani, D. C., Ryter, S. W., Baron, R. M., and Choi, A. M. (2012) Inflammasome-regulated cytokines are critical mediators of acute lung injury. Am. J. Respir. Crit. Care Med. 185, 1225-1234
4. Bauernfeind, F. G., Horvath, G., Stutz, A., Alnemri, E. S., MacDonald, K., Speert, D., Fernandes-Alnemri, T., Wu, J., Monks, B. G., Fitzgerald, K. A., Hornung, V., and Latz, E. (2009) Cutting edge: NF-κB activating pattern recognition and cytokine receptors license NLRP3 inflammasome activation by regulating NLRP3 expression. J. Immunol. 183, 787-791
5. Hershko, A., and Ciechanover, A. (1998) The ubiquitin system. Annu. Rev. Biochem. 67, 425-479
6. Deshaies, R. J., and Joazeiro, C. A. (2009) RING domain E3 ubiquitin ligases. Annu. Rev. Biochem. 78, 399-434
7. Cardozo, T., and Pagano, M. (2004) The SCF ubiquitin ligase: insights into a molecular machine. Nat. Rev. Mol. Cell Biol. 5, 739-751
8. Chen, B. B., Coon, T. A., Glasser, J. R., McVerry, B. J., Zhao, J., Zhao, Y., Zou, C., Ellis, B., Sciurba, F. C., Zhang, Y., and Mallampalli, R. K. (2013) A combinatorial F box protein directed pathway controls TRAF adaptor stability to regulate inflammation. Nat. Immunol. 14, 470-479
9. Davies, J. Q., and Gordon, S. (2005) Isolation and culture of human macrophages. Methods Mol. Biol. 290, 105-116
10. Chen, B. B., and Mallampalli, R. K. (2009) Masking of a nuclear signal motif by monoubiquitination leads to mislocalization and degradation of the regulatory enzyme cytidylyltransferase. Mol. Cell. Biol. 29, 3062-3075
11. Mallampalli, R. K., Coon, T. A., Glasser, J. R., Wang, C., Dunn, S. R., Weathington, N. M., Zhao, J., Zou, C., Zhao, Y., and Chen, B. B. (2013) Targeting F box protein Fbxo3 to control cytokine-driven inflammation. J. Immunol. 191, 5247-5255
12. Radivojac, P., Vacic, V., Haynes, C., Cocklin, R. R., Mohan, A., Heyen, J. W., Goebl, M. G., and Iakoucheva, L. M. (2010) Identification, analysis, and prediction of protein ubiquitination sites. Proteins 78, 365-380
13. Schroder, K., and Tschopp, J. (2010) The inflammasomes. Cell 140, 821-832
14. Juliana, C., Fernandes-Alnemri, T., Kang, S., Farias, A., Qin, F., and Alnemri, E. S. (2012) Non-transcriptional priming and deubiquitination regulate NLRP3 inflammasome activation. J. Biol. Chem. 287, 36617-36622
15. Fernandes-Alnemri, T., Kang, S., Anderson, C., Sagara, J., Fitzgerald, K. A., and Alnemri, E. S. (2013) Cutting edge: TLR signaling licenses IRAK1 for rapid activation of the NLRP3 inflammasome. J. Immunol. 191, 3995-3999
16. Niebler, M., Qian, X., Höfler, D., Kogosov, V., Kaewprag, J., Kaufmann, A. M., Ly, R., Böhmer, G., Zawatzky, R., Rösl, F., and Rincon-Orozco, B. (2013) Post-translational control of IL-1β via the human papillomavirus type 16 E6 oncoprotein: a novel mechanism of innate immune escape mediated by the E3-ubiquitin ligase E6-AP and p53. PLoS Pathog. 9, e1003536
17. Ghonime, M. G., Shamaa, O. R., Das, S., Eldomany, R. A., Fernandes- Alnemri, T., Alnemri, E. S., Gavrilin, M. A., and Wewers, M. D. (2014) Inflammasome priming by lipopolysaccharide is dependent upon ERK signaling and proteasome function. J. Immunol. 192, 3881-3888
18. Hu, Y., Nguyen, T. T., Bui, K. C., Demello, D. E., and Smith, J. B. (2005) A novel inflammation-induced ubiquitin E3 ligase in alveolar type II cells. Biochem. Biophys. Res. Commun. 333, 253-263
19. Mayor, A., Martinon, F., De Smedt, T., Pétrilli, V., and Tschopp, J. (2007) A crucial function of SGT1 and HSP90 in inflammasome activity links mammalian and plant innate immune responses. Nat. Immunol. 8, 497-503
20. Lopez-Castejon, G., Luheshi, N. M., Compan, V., High, S., Whitehead, R. C., Flitsch, S., Kirov, A., Prudovsky, I., Swanton, E., and Brough, D. (2013) Deubiquitinases regulate the activity of caspase-1 and interleukin-1β secretion via assembly of the inflammasome. J. Biol. Chem. 288, 2721-2733
21. Py, B. F., Kim, M. S., Vakifahmetoglu-Norberg, H., and Yuan, J. (2013) Deubiquitination of NLRP3 by BRCC3 critically regulates inflammasome activity. Mol. Cell 49, 331-338
22. Weng, L., Mitoma, H., Trichot, C., Tricot, C., Bao, M., Liu, Y., Zhang, Z., and Liu, Y. J. (2014) The E3 ubiquitin ligase tripartite motif 33 is essential for cytosolic RNA-induced NLRP3 inflammasome activation. J. Immunol. 193, 3676-3682
23. Rodgers, M. A., Bowman, J. W., Fujita, H., Orazio, N., Shi, M., Liang, Q., Amatya, R., Kelly, T. J., Iwai, K., Ting, J., and Jung, J. U. (2014) The linear ubiquitin assembly complex (LUBAC) is essential for NLRP3 inflammasome activation. J. Exp. Med. 211, 1333-1347
24. Yan, Y., Jiang, W., Liu, L., Wang, X., Ding, C., Tian, Z., and Zhou, R. (2015) Dopamine controls systemic inflammation through inhibition of NLRP3 inflammasome. Cell 160, 62-73
25. Zhu, L. J., Yang, X., Li, X. Y., Liu, Q. H., Tang, X. Q., Zhou, S. F., Kong, Q. Y., Axelsson, J., and Yu, X. Q. (2010) Suppression of tumor necrosis factor receptor associated factor (TRAF)-2 attenuates the proinflammatory and proliferative effect of aggregated IgG on rat renal mesangial cells. Cytokine 49, 201-208