Alternative inflammasome activation enables IL-1β release from living cells

Current Opinion in Immunology

Volumn 44, Issue , 2017, Pages 7-13

  Gaidt, Moritz M ^a   Hornung, Veit ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 11; CASPASE 4; CASPASE 5; CASPASE 8; CELL CYCLE PROTEIN; CRYOPYRIN; EFFECTOR CASPASE; GASDERMIN D; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INFLAMMASOME; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; LIPOPOLYSACCHARIDE; MEMBRANE LIPID; NEK7 PROTEIN; OXPAPC; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR RECEPTOR; UNCLASSIFIED DRUG; POTASSIUM PROTON EXCHANGE PROTEIN;

APOPTOSIS; AUTOPHAGY; CELL MEMBRANE; CYTOKINE RELEASE; DENDRITIC CELL; ENZYME ACTIVATION; HOMEOSTASIS; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; INFLAMMATION; MONOCYTE; POTASSIUM TRANSPORT; PROTEIN EXPRESSION; PROTEIN PROCESSING; PYROPTOSIS; REVIEW; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; IMMUNOLOGY; METABOLISM;

ANIMALS; CASPASE 8; HOMEOSTASIS; HUMANS; INFLAMMASOMES; INFLAMMATION; INTERLEUKIN-1BETA; LIPOPOLYSACCHARIDES; NLR FAMILY, PYRIN DOMAIN-CONTAINING 3 PROTEIN; POTASSIUM-HYDROGEN ANTIPORTERS; PYROPTOSIS; SIGNAL TRANSDUCTION;

EID: 84994791054     PISSN: 09527915     EISSN: 18790372     Source Type: Journal    
DOI: 10.1016/j.coi.2016.10.007     Document Type: Review

References (59)

1. 1 Dinarello, C.A., Immunological and inflammatory functions of the interleukin-1 family. Annu Rev Immunol 27 (2009), 519–550.
2. 2 Dinarello, C.A., A clinical perspective of IL-1b as the gatekeeper of inflammation. Eur J Immunol 41 (2011), 1203–1217.
3. 3 Garlanda, C., Dinarello, C.A., Mantovani, A., The Interleukin-1 family: back to the future [Internet]. Immunity 39 (2013), 1003–1018.
4. 4 Fernandes-Alnemri, T., Wu, J., Yu, J.-W., Datta, P., Miller, B., Jankowski, W., Rosenberg, S., Zhang, J., Alnemri, E.S., The pyroptosome: a supramolecular assembly of ASC dimers mediating inflammatory cell death via caspase-1 activation. Cell Death Differ. 14 (2007), 1590–1604.
5. 5•• Shi, J., Zhao, Y., Wang, K., Shi, X., Wang, Y., Huang, H., Zhuang, Y., Cai, T., Wang, F., Shao, F., Cleavage of GSDMD by inflammatory caspases determines pyroptotic cell death. Nature 526 (2015), 660–665 This is one of three reports identifying a crucial role for GSDMD in pyroptosis that is regulated by proteolytic cleavage by inflammatory caspases.
6. ••].
7. ••].
8. 8 Sborgi, L., Rühl, S., Mulvihill, E., Pipercevic, J., Heilig, R., GSDMD pore formation in the plasma membrane constitutes the mechanism of pyroptotic cell death. EMBO J, 2016, 10.15252/embj.201694696.
9. 9 Aglietti, R.A., Estevez, A., Gupta, A., Ramirez, M.G., Liu, P.S., Kayagaki, N., Ciferri, C., Dixit, V.M., Dueber, E.C., GsdmD p30 elicited by caspase-11 during pyroptosis forms pores in membranes. Proc Natl Acad Sci 113 (2016), 7858–7863.
10. 10• Ding, J., Wang, K., Liu, W., She, Y., Sun, Q., Shi, J., Sun, H., Wang, D.-C., Shao, F., Pore-forming activity and structural autoinhibition of the gasdermin family. Nature 535 (2016), 111–116 This paper identifies pore formation by GSDMD as the effector mechanism of pyroptosis.
11. 11 Liu, X., Zhang, Z., Ruan, J., Pan, Y., Magupalli, V.G., Wu, H., Lieberman, J., Inflammasome-activated gasdermin D causes pyroptosis by forming membrane pores. Nature 535 (2016), 153–158.
12. 12 Jorgensen, I., Zhang, Y., Krantz, B.A., Miao, E.A., Pyroptosis triggers pore-induced intracellular traps (PITs) that capture bacteria and lead to their clearance by efferocytosis [Internet]. J Exp Med, 2016, 10.1084/jem.20151613.
13. 13 Martín-sánchez, F., Diamond, C., Zeitler, M., Gomez-sanchez, A., Peñalver, M., Paszek, P., Steringer, J.P., Nickel, W., Inflammasome-dependent IL-1 β release depends upon membrane permeabilisation. Cell Death Differ, 2016, 10.1038/cdd.2015.176.
14. 14 Liu, T., Yamaguchi, Y., Shirasaki, Y., Shikada, K., Yamagishi, M., Hoshino, K., Kaisho, T., Takemoto, K., Suzuki, T., Kuranaga, E., et al. Single-cell imaging of caspase-1 dynamics reveals an all-or-none inflammasome signaling response [Internet]. Cell Rep 8 (2013), 974–982.
15. 15 Hoffman, H.M., Mueller, J.L., Broide, D.H., Wanderer, A.A., Kolodner, R.D., Mutation of a new gene encoding a putative pyrin-like protein causes familial cold autoinflammatory syndrome and Muckle-Wells syndrome. [Internet]. Nat Genet 29 (2001), 301–305.
16. 16 Coll, R.C., Robertson, A.A.B., Chae, J.J., Higgins, S.C., Muñoz-Planillo, R., Inserra, M.C., Vetter, I., Dungan, L.S., Monks, B.G., Stutz, A., et al. A small-molecule inhibitor of the NLRP3 inflammasome for the treatment of inflammatory diseases. [Internet]. Nat Med 21 (2015), 248–255.
17. 17 van Hout, G.P.J., Bosch, L., Ellenbroek, G.H.J.M., de Haan, J.J., van Solinge, W.W., Cooper, M.A., Arslan, F., de Jager, S.C.A., Robertson, A.A.B., Pasterkamp, G., et al. The selective NLRP3-inflammasome inhibitor MCC950 reduces infarct size and preserves cardiac function in a pig model of myocardial infarction. [Internet]. Eur Heart J, 2016, 10.1093/eurheartj/ehw247.
18. 18 Primiano, M.J., Lefker, B.A., Bowman, M.R., Bree, A.G., Hubeau, C., Bonin, P.D., Mangan, M., Dower, K., Monks, B.G., Cushing, L., et al. Efficacy and pharmacology of the NLRP3 inflammasome inhibitor CP-456,773 (CRID3) in murine models of dermal and pulmonary inflammation [Internet]. J Immunol, 2016, 773.
19. 19 Tate, M.D., Ong, J.D.H., Dowling, J.K., McAuley, J.L., Robertson, A.B., Latz, E., Drummond, G.R., Cooper, M.A., Hertzog, P.J., Mansell, A., Reassessing the role of the NLRP3 inflammasome during pathogenic influenza A virus infection via temporal inhibition. [Internet]. Sci Rep, 6, 2016, 27912.
20. 20 Pétrilli, 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 14 (2007), 1583–1589.
21. + efflux is the common trigger of NLRP3 inflammasome activation by bacterial toxins and particulate matter. [Internet]. Immunity 38 (2013), 1142–1153.
22. 22 Schmid-Burgk, J.L., Chauhan, D., Schmidt, T., Ebert, T.S., Reinhardt, J., Endl, E., Hornung, V., A genome-wide CRISPR screen identifies NEK7 as an essential component of NLRP3 inflammasome activation. [Internet]. J Biol Chem 291 (2016), 103–109.
23. 23 He, Y., Zeng, M.Y., Yang, D., Motro, B., Núñez, G., Nek7 is an essential mediator of NLRP3 oligomerization and inflammasome activation downstream of potassium efflux [Internet]. Nature 530 (2016), 354–357.
24. 24 Shi, H., Wang, Y., Li, X., Zhan, X., Tang, M., Fina, M., Su, L., Pratt, D., Bu, C.H., Hildebrand, S., et al. NLRP3 activation and mitosis are mutually exclusive events coordinated by NEK7, a new inflammasome component [Internet]. Nat Immunol 17 (2015), 1–12.
25. 25 Kayagaki, N., Noncanonical inflammasome activation by intracellular LPS independent of TLR4. Science, 2014, 1246.
26. 26 Hagar, J.A., Powell, D.A., Aachoui, Y., Ernst, R.K., Miao, E.A., Cytoplasmic LPS activates caspase-11: implications in TLR4-independent endotoxic shock. [Internet]. Science 341 (2013), 1250–1253.
27. 27 Shi, J., Zhao, Y., Wang, Y., Gao, W., Ding, J., Li, P., Hu, L., Shao, F., Inflammatory caspases are innate immune receptors for intracellular LPS. Nature 514 (2014), 187–192.
28. 28 Schmid-Burgk, J.L., Gaidt, M.M., Schmidt, T., Ebert, T.S., Bartok, E., Hornung, V., Caspase-4 mediates non-canonical activation of the NLRP3 inflammasome in human myeloid cells. Eur J Immunol 45 (2015), 2911–2917.
29. 29 Rühl, S., Broz, P., Caspase-11 activates a canonical NLRP3 inflammasome by promoting K+ efflux [Internet]. Eur J Immunol 45 (2015), 2927–2936.
30. 30 Baker, P.J., Boucher, D., Bierschenk, D., Tebartz, C., Whitney, P.G., D'Silva, D.B., Tanzer, M.C., Monteleone, M., Robertson, A.A.B., Cooper, M.A., et al. NLRP3 inflammasome activation downstream of cytoplasmic LPS recognition by both caspase-4 and caspase-5. [Internet]. Eur J Immunol 45 (2015), 2918–2926.
31. 31•• Gaidt, M.M., Ebert, T.S., Chauhan, D., Schmidt, T., Schmid-Burgk, J.L., Rapino, F., Robertson, A.A.B., Cooper, M.A., Graf, T., Hornung, V., Human monocytes engage an alternative inflammasome pathway. Immunity 44 (2016), 833–846 First characterization of the alternative inflammasome by genetic means and phenotypic description.
32. 32• Felley, L.E., Sharma, A., Theisen, E., James, C., Sauer, J., Gumperz, J.E., Human invariant NKT cells induce IL-1 β secretion by peripheral blood monocytes via a P2X 7-independent pathway. J Immunol, 2016, 10.4049/jimmunol.1600790 Description of alternative inflammasome signaling by sensing iNKT cell derived signals.
33. 33 Lemmers, B., Salmena, L., Bidere, N., Su, H., Matysiak-Zablocki, E., Murakami, K., Ohashi, P.S., Jurisicova, A., Lenardo, M., Hakem, R., et al. Essential role for caspase-8 in toll-like receptors and NFkB signaling. J Biol Chem 282 (2007), 7416–7423.
34. 34 Su, H., Bidère, N., Zheng, L., Cubre, A., Sakai, K., Dale, J., Salmena, L., Hakem, R., Straus, S., Lenardo, M., Requirement for caspase-8 in NF-kappaB activation by antigen receptor. [Internet]. Science 307 (2005), 1465–1468.
35. 35 Gurung, P., Anand, P.K., Malireddi, R.K.S., Vande Walle, L., Van Opdenbosch, N., Dillon, C.P., Weinlich, R., Green, D.R., Lamkanfi, M., Kanneganti, T.-D., FADD and caspase-8 mediate priming and activation of the canonical and noncanonical Nlrp3 inflammasomes [Internet]. J Immunol 192 (2014), 1835–1846.
36. 36 Allam, R., Lawlor, K.E., Yu, E.C.-W., Mildenhall, A.L., Moujalled, D.M., Lewis, R.S., Ke, F., Mason, K.D., White, M.J., Stacey, K.J., et al. Mitochondrial apoptosis is dispensable for NLRP3 inflammasome activation but non-apoptotic caspase-8 is required for inflammasome priming. [Internet]. EMBO Rep 15 (2014), 1–9.
37. 37 Kang, S., Fernandes-Alnemri, T., Rogers, C., Mayes, L., Wang, Y., Dillon, C., Roback, L., Kaiser, W., Oberst, A., Sagara, J., et al. Caspase-8 scaffolding function and MLKL regulate NLRP3 inflammasome activation downstream of TLR3 [Internet]. Nat Commun, 6, 2015, 7515.
38. 38 Man, S.M., Tourlomousis, P., Hopkins, L., Monie, T.P., Fitzgerald, K.A., Bryant, C.E., Salmonella infection induces recruitment of Caspase-8 to the inflammasome to modulate IL-1beta production [Internet]. J Immunol 191 (2013), 5239–5246.
39. 39 Vajjhala, P.R., Lu, A., Brown, D.L., Pang, S.W., Sagulenko, V., Sester, D.P., Cridland, S.O., Hill, J.M., Schroder, K., Stow, J.L., et al. The inflammasome adaptor ASC induces procaspase-8 death effector domain filaments. J Biol Chem 290 (2015), 29217–29230.
40. 40 Maelfait, J., Vercammen, E., Janssens, S., Schotte, P., Haegman, M., Magez, S., Beyaert, R., Stimulation of Toll-like receptor 3 and 4 induces interleukin-1beta maturation by caspase-8. [Internet]. J Exp Med 205 (2008), 1967–1973.
41. 41 Lawlor, K.E., Khan, N., Mildenhall, A., Gerlic, M., Croker, B.a., D'Cruz, A.a., Hall, C., Kaur Spall, S., Anderton, H., Masters, S.L., et al. RIPK3 promotes cell death and NLRP3 inflammasome activation in the absence of MLKL [Internet]. Nat Commun, 6, 2015, 6282.
42. 42•• Zanoni, I., Tan, Y., Gioia, M. Di, Broggi, A., Ruan, J., Shi, J., Donado, C.A., Shao, F., Wu, H., Springstead, J.R., et al. An endogenous caspase-11 ligand elicits interleukin-1 release from living dendritic cells. Science 352 (2016), 1232–1236 Examines an oxPAPC-induced inflammamasome pathway with similar features compared to alternative inflammasome activation.
43. 43•• Wolf, A.J., Reyes, C.N., Liang, W., Becker, C., Shimada, K., Wheeler, M.L., Cho, H.C., Popescu, N.I., Coggeshall, K.M., Arditi, M., et al. Hexokinase is an innate immune receptor for the detection of bacterial peptidoglycan. Cell 116 (2016), 1–13 This paper reports that metabolic perturbations leading to hexokinase translocation into the cytosol trigger inflammasome activation resembling alternative inflammasome activation.
44. 44 Majewski, N., Nogueira, V., Bhaskar, P., Coy, P.E., Skeen, J.E., Gottlob, K., Chandel, N.S., Thompson, C.B., Robey, R.B., Hay, N., Hexokinase-mitochondria interaction mediated by Akt is required to inhibit apoptosis in the presence or absence of Bax and Bak. Mol Cell 16 (2004), 819–830.
45. 45 Kruidering, M., Evan, G.I., Caspase-8 in apoptosis: the beginning of “the end”? [Internet]. IUBMB Life 50 (2000), 85–90.
46. 46 Lopez-Castejon, G., Brough, D., Understanding the mechanism of IL-1β secretion [Internet]. Cytokine Growth Factor Rev 22 (2011), 189–195.
47. 47 Rubartelli, A., Cozzolino, F., Talio, M., Sitia, R., A novel secretory pathway for interleukin-1 beta, a protein lacking a signal sequence. [Internet]. EMBO J 9 (1990), 1503–1510.
48. 48• Zhang, M., Sam, K., Ge, L., Xu, K., Schekman, R., Translocation of interleukin-1β into a vesicle intermediate in autophagy-mediated secretion. Elife, 4, 2015, e11205 Elegant demonstration that unconventional IL-1β secretion requires autophagy-assisted entry into the exocytotic pathway upon Caspase-1 activation in pyroptosis incompetent cells.
49. 49 Chen, K.W., Groß, C.J., Sotomayor, F., Stacey, K.J., Tschopp, J., Sweet, M.J., Schroder, K., The neutrophil NLRC4 inflammasome selectively promotes IL-1β maturation without pyroptosis during acute Salmonella challenge. Cell Rep 8 (2014), 570–582.
50. 50 Miao, E., Rajan, J., Aderem, A., Caspase-1 induced pyroptotic cell death. Immunol Rev 243 (2013), 206–214.
51. 51 Pioli, P.A., Weaver, L.K., Schaefer, T.M., Wright, J.a., Wira, C.R., Guyre, P.M., Lipopolysaccharide-induced IL-1 beta production by human uterine macrophages up-regulates uterine epithelial cell expression of human beta-defensin 2. J Immunol 176 (2006), 6647–6655.
52. 52 Wewers, M.D., Herzyk, D.J., Alveolar macrophages differ from blood monocytes in human IL-1 beta release. Quantitation by enzyme-linked immunoassay [Internet]. J Immunol 143 (1989), 1635–1641.
53. 53 Yu, M., Wang, H., Ding, A., Golenbock, D.T., Latz, E., Czura, C.J., Fenton, M.J., Tracey, K.J., Yang, H., Hmgb1 signals through toll-like receptor (Tlr) 4 and Tlr2 [Internet]. Shock 26 (2006), 174–179.
54. 54 Vabulas, R.M., Ahmad-Nejad, P., Da Costa, C., Miethke, T., Kirschning, C.J., Häcker, H., Wagner, H., Endocytosed HSP60s use toll-like receptor 2 (TLR2) and TLR4 to activate the toll/interleukin-1 receptor signaling pathway in innate immune cells. J Biol Chem 276 (2001), 31332–31339.
55. 55 Jiang, D., Liang, J., Fan, J., Yu, S., Chen, S., Luo, Y., Prestwich, G.D., Mascarenhas, M.M., Garg, H.G., Quinn, D.A., et al. Regulation of lung injury and repair by Toll-like receptors and hyaluronan [Internet]. Nat Med 11 (2005), 1173–1179.
56. 56 Schaefer, L., Babelova, A., Kiss, E., Hausser, H.J., Baliova, M., Krzyzankova, M., Marsche, G., Young, M.F., Mihalik, D., G?.?.tte, M., et al. The matrix component biglycan is proinflammatory and signals through Toll-like receptors 4 and 2 in macrophages. J Clin Invest 115 (2005), 2223–2233.
57. 57 Johnson, G.B., Brunn, G.J., Kodaira, Y., Platt, J.L., Receptor-mediated monitoring of tissue well-being via detection of soluble heparan sulfate by Toll-like receptor 4. J Immunol 168 (2002), 5233–5239.
58. 58 Vogl, T., Tenbrock, K., Ludwig, S., Leukert, N., Ehrhardt, C., van Zoelen, M.a.D., Nacken, W., Foell, D., van der Poll, T., Sorg, C., et al. Mrp8 and Mrp14 are endogenous activators of Toll-like receptor 4, promoting lethal, endotoxin-induced shock. Nat Med 13 (2007), 1042–1049.
59. 59 Chen, G.Y., Nuñez, G., Sterile inflammation: sensing and reacting to damage. Nat Rev Immunol 10 (2010), 826–837.