Interleukin-1β Maturation Triggers Its Relocation to the Plasma Membrane for Gasdermin-D-Dependent and -Independent Secretion

Cell Reports

Volumn 24, Issue 6, 2018, Pages 1425-1433

  Monteleone, Mercedes ^a   Stanley, Amanda C ^a,b   Chen, Kaiwen W ^a,c   Brown, Darren L ^a   Bezbradica, Jelena S ^a,d   von Pein, Jessica B ^a   Holley, Caroline L ^a   Boucher, Dave ^a,c   Shakespear, Melanie R ^a   Kapetanovic, Ronan ^a   Rolfes, Verena ^a,e   Sweet, Matthew J ^a   Stow, Jennifer L ^a   Schroder, Kate ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^c UNIVERSITY OF LAUSANNE   (Switzerland)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e UNIVERSITY HOSPITAL BONN   (Germany)

Author keywords

caspase 1; gasdermin; inflammasome; interleukin 1; macrophage; neutrophil; phosphoinositides; pyroptosis; trafficking; unconventional protein secretion

Indexed keywords

CELL PROTEIN; GASDERMIN D; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; UNCLASSIFIED DRUG; GSDMD PROTEIN, HUMAN; PHOSPHATE BINDING PROTEIN; SIGNAL PEPTIDE;

ANIMAL CELL; ARTICLE; BONE MARROW CELL; CELL MEMBRANE; CONTROLLED STUDY; CYTOKINE RELEASE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROCESSING; PROTEIN SECRETION; PROTEIN TRANSPORT; GENETIC TRANSFECTION; METABOLISM;

CELL MEMBRANE; HUMANS; INTERLEUKIN-1BETA; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; PHOSPHATE-BINDING PROTEINS; TRANSFECTION;

EID: 85050821468     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2018.07.027     Document Type: Article

References (42)

1. 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. USA 113 (2016), 7858–7863.
2. Bohdanowicz, M., Grinstein, S., Role of phospholipids in endocytosis, phagocytosis, and macropinocytosis. Physiol. Rev. 93 (2013), 69–106.
3. Boucher, D., Monteleone, M., Coll, R.C., Chen, K.W., Ross, C.M., Teo, J.L., Gomez, G.A., Holley, C.L., Bierschenk, D., Stacey, K.J., et al. Caspase-1 self-cleavage is an intrinsic mechanism to terminate inflammasome activity. J. Exp. Med. 215 (2018), 827–840.
4. Brough, D., Rothwell, N.J., Caspase-1-dependent processing of pro-interleukin-1β is cytosolic and precedes cell death. J. Cell Sci. 120 (2007), 772–781.
5. Chen, K.W., Groß, C.J., Sotomayor, F.V., 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.
6. Conos, S.A., Lawlor, K.E., Vaux, D.L., Vince, J.E., Lindqvist, L.M., Cell death is not essential for caspase-1-mediated interleukin-1β activation and secretion. Cell Death Differ. 23 (2016), 1827–1838.
7. Conos, S.A., Chen, K.W., De Nardo, D., Hara, H., Whitehead, L., Núñez, G., Masters, S.L., Murphy, J.M., Schroder, K., Vaux, D.L., et al. Active MLKL triggers the NLRP3 inflammasome in a cell-intrinsic manner. Proc. Natl. Acad. Sci. USA 114 (2017), E961–E969.
8. Cullen, S.P., Kearney, C.J., Clancy, D.M., Martin, S.J., Diverse activators of the NLRP3 inflammasome promote IL-1β secretion by triggering necrosis. Cell Rep. 11 (2015), 1535–1548.
9. Diamond, C.E., Leong, K.W.K., Vacca, M., Rivers-Auty, J., Brough, D., Mortellaro, A., Salmonella typhimurium-induced IL-1 release from primary human monocytes requires NLRP3 and can occur in the absence of pyroptosis. Sci. Rep., 7, 2017, 6861.
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.
11. Dupont, N., Jiang, S., Pilli, M., Ornatowski, W., Bhattacharya, D., Deretic, V., Autophagy-based unconventional secretory pathway for extracellular delivery of IL-1β. EMBO J. 30 (2011), 4701–4711.
12. Evavold, C.L., Ruan, J., Tan, Y., Xia, S., Wu, H., Kagan, J.C., The pore-forming protein gasdermin D regulates interleukin-1 secretion from living macrophages. Immunity 48 (2018), 35–44.e6.
13. Fink, S.L., Cookson, B.T., Caspase-1-dependent pore formation during pyroptosis leads to osmotic lysis of infected host macrophages. Cell. Microbiol. 8 (2006), 1812–1825.
14. Gaidt, M.M., Ebert, T.S., Chauhan, D., Schmidt, T., Schmid-Burgk, J.L., Rapino, F., Robertson, A.A., Cooper, M.A., Graf, T., Hornung, V., Human monocytes engage an alternative inflammasome pathway. Immunity 44 (2016), 833–846.
15. Gross, O., Measuring the inflammasome. Methods Mol. Biol. 844 (2012), 199–222.
16. Gutierrez, K.D., Davis, M.A., Daniels, B.P., Olsen, T.M., Ralli-Jain, P., Tait, S.W., Gale, M. Jr., Oberst, A., MLKL activation triggers NLRP3-mediated processing and release of IL-1β independently of gasdermin-D. J. Immunol. 198 (2017), 2156–2164.
17. He, W.T., Wan, H., Hu, L., Chen, P., Wang, X., Huang, Z., Yang, Z.H., Zhong, C.Q., Han, J., Gasdermin D is an executor of pyroptosis and required for interleukin-1β secretion. Cell Res. 25 (2015), 1285–1298.
18. Kang, T.B., Yang, S.H., Toth, B., Kovalenko, A., Wallach, D., Caspase-8 blocks kinase RIPK3-mediated activation of the NLRP3 inflammasome. Immunity 38 (2013), 27–40.
19. Karmakar, M., Katsnelson, M., Malak, H.A., Greene, N.G., Howell, S.J., Hise, A.G., Camilli, A., Kadioglu, A., Dubyak, G.R., Pearlman, E., Neutrophil IL-1β processing induced by pneumolysin is mediated by the NLRP3/ASC inflammasome and caspase-1 activation and is dependent on K+ efflux. J. Immunol. 194 (2015), 1763–1775.
20. Kayagaki, N., Stowe, I.B., Lee, B.L., O'Rourke, K., Anderson, K., Warming, S., Cuellar, T., Haley, B., Roose-Girma, M., Phung, Q.T., et al. Caspase-11 cleaves gasdermin D for non-canonical inflammasome signalling. Nature 526 (2015), 666–671.
21. Kuida, K., Lippke, J.A., Ku, G., Harding, M.W., Livingston, D.J., Su, M.S., Flavell, R.A., Altered cytokine export and apoptosis in mice deficient in interleukin-1 beta converting enzyme. Science 267 (1995), 2000–2003.
22. Lawlor, K.E., Feltham, R., Yabal, M., Conos, S.A., Chen, K.W., Ziehe, S., Graß, C., Zhan, Y., Nguyen, T.A., Hall, C., et al. XIAP loss triggers RIPK3- and caspase-8-driven IL-1β activation and cell death as a consequence of TLR-MyD88-induced cIAP1-TRAF2 degradation. Cell Rep. 20 (2017), 668–682.
23. 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. Cell Rep. 8 (2014), 974–982.
24. 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.
25. Martín-Sánchez, F., Diamond, C., Zeitler, M., Gomez, A.I., Baroja-Mazo, A., Bagnall, J., Spiller, D., White, M., Daniels, M.J., Mortellaro, A., et al. Inflammasome-dependent IL-1β release depends upon membrane permeabilisation. Cell Death Differ. 23 (2016), 1219–1231.
26. Monteleone, M., Stow, J.L., Schroder, K., Mechanisms of unconventional secretion of IL-1 family cytokines. Cytokine 74 (2015), 213–218.
27. Pelegrin, P., Barroso-Gutierrez, C., Surprenant, A., P2X7 receptor differentially couples to distinct release pathways for IL-1beta in mouse macrophage. J. Immunol. 180 (2008), 7147–7157.
28. Sborgi, L., Rühl, S., Mulvihill, E., Pipercevic, J., Heilig, R., Stahlberg, H., Farady, C.J., Müller, D.J., Broz, P., Hiller, S., GSDMD membrane pore formation constitutes the mechanism of pyroptotic cell death. EMBO J. 35 (2016), 1766–1778.
29. Schroder, K., Tschopp, J., The inflammasomes. Cell 140 (2010), 821–832.
30. Schroder, K., Irvine, K.M., Taylor, M.S., Bokil, N.J., Le Cao, K.A., Masterman, K.A., Labzin, L.I., Semple, C.A., Kapetanovic, R., Fairbairn, L., et al. Conservation and divergence in Toll-like receptor 4-regulated gene expression in primary human versus mouse macrophages. Proc. Natl. Acad. Sci. USA 109 (2012), E944–E953.
31. Schroder, K., Sagulenko, V., Zamoshnikova, A., Richards, A.A., Cridland, J.A., Irvine, K.M., Stacey, K.J., Sweet, M.J., Acute lipopolysaccharide priming boosts inflammasome activation independently of inflammasome sensor induction. Immunobiology 217 (2012), 1325–1329.
32. 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.
33. Shirasaki, Y., Yamagishi, M., Suzuki, N., Izawa, K., Nakahara, A., Mizuno, J., Shoji, S., Heike, T., Harada, Y., Nishikomori, R., Ohara, O., Real-time single-cell imaging of protein secretion. Sci. Rep., 4, 2014, 4736.
34. Stoffels, M., Zaal, R., Kok, N., van der Meer, J.W., Dinarello, C.A., Simon, A., ATP-induced IL-1β specific secretion: true under stringent conditions. Front. Immunol., 6, 2015, 54.
35. Taabazuing, C.Y., Okondo, M.C., Bachovchin, D.A., Pyroptosis and apoptosis pathways engage in bidirectional crosstalk in monocytes and macrophages. Cell Chem. Biol. 24 (2017), 507–514.e504.
36. Verhoef, P.A., Kertesy, S.B., Estacion, M., Schilling, W.P., Dubyak, G.R., Maitotoxin induces biphasic interleukin-1beta secretion and membrane blebbing in murine macrophages. Mol. Pharmacol. 66 (2004), 909–920.
37. Viganò, E., Diamond, C.E., Spreafico, R., Balachander, A., Sobota, R.M., Mortellaro, A., Human caspase-4 and caspase-5 regulate the one-step non-canonical inflammasome activation in monocytes. Nat. Commun., 6, 2015, 8761.
38. 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., Underhill, D.M., Hexokinase is an innate immune receptor for the detection of bacterial peptidoglycan. Cell 166 (2016), 624–636.
39. Yeo, J.C., Wall, A.A., Luo, L., Condon, N.D., Stow, J.L., Distinct roles for APPL1 and APPL2 in regulating Toll-like receptor 4 signaling in macrophages. Traffic 17 (2016), 1014–1026.
40. Yoon, S., Kovalenko, A., Bogdanov, K., Wallach, D., MLKL, the protein that mediates necroptosis, also regulates endosomal trafficking and extracellular vesicle generation. Immunity 47 (2017), 51–65.e57.
41. Zanoni, I., Tan, Y., Di Gioia, M., Broggi, A., Ruan, J., Shi, J., Donado, C.A., Shao, F., Wu, H., Springstead, J.R., Kagan, J.C., An endogenous caspase-11 ligand elicits interleukin-1 release from living dendritic cells. Science 352 (2016), 1232–1236.
42. Zhang, M., Kenny, S.J., Ge, L., Xu, K., Schekman, R., Translocation of interleukin-1β into a vesicle intermediate in autophagy-mediated secretion. eLife, 4, 2015, e11205.