The Gasdermin-D pore acts as a conduit for IL-1β secretion in mice

European Journal of Immunology

Volumn 48, Issue 4, 2018, Pages 584-592

  Heilig, Rosalie ^a,c   Dick, Mathias S ^a   Sborgi, Lorenzo ^a   Meunier, Etienne ^b   Hiller, Sebastian ^a   Broz, Petr ^a,c  

^a UNIVERSITY OF BASEL   (Switzerland)

^b UNIVERSITÉ DE TOULOUSE   (France)

^c UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

Gasdermin D pore; Inflammasome; Interleukin 1 ; Pyroptosis; Unconventional protein secretion

Indexed keywords

AIM2 PROTEIN; ALARMIN; ALPHA TUBULIN; CASPASE 11; CRYOPYRIN; GASDERMIN D; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HIGH MOBILITY GROUP B1 PROTEIN; INFLAMMASOME; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; LACTATE DEHYDROGENASE; LIPOSOME; MEMBRANE PROTEIN; MESSENGER RNA; NLRC4 PROTEIN; PEPTIDES AND PROTEINS; PROTEIN P20; RAC1 PROTEIN; UNCLASSIFIED DRUG; APOPTOSIS REGULATORY PROTEIN; CASP1 PROTEIN, MOUSE; GSDMD PROTEIN, MOUSE; IL1B PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BONE MARROW DERIVED DENDRITIC CELL; BONE MARROW DERIVED MACROPHAGE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; CYTOLYSIS; CYTOSOL; IN VITRO STUDY; MOUSE; MRNA EXPRESSION LEVEL; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PYROPTOSIS; TRANSPORT ASSAY; ANIMAL; CELL CULTURE; DENDRITIC CELL; GENETICS; KNOCKOUT MOUSE; MACROPHAGE; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT;

ANIMALS; APOPTOSIS REGULATORY PROTEINS; CASPASE 1; CELLS, CULTURED; DENDRITIC CELLS; INTERLEUKIN-1BETA; LIPOSOMES; MACROPHAGES; MICE; MICE, KNOCKOUT; PROTEIN TRANSPORT; PYROPTOSIS;

EID: 85040539132     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201747404     Document Type: Article

References (53)

1. Dinarello, C. A., Interleukin-1. Cytokine Growth Factor Rev. 1997. 8: 122–132.
2. Dinarello, C. A., Interleukin-1 and the pathogenesis of the acute-phase response. N. Engl. J. Med. 1984. 311: 1413–1418.
3. Garlanda, C., Dinarello, C. A., and Mantovani, A., The interleukin-1 family: back to the future. Immunity. 2013. 39: 1003–1018.
4. Palomo, J., Dietrich, D., Martin, P., Palmer, G., and Gabay, C., The interleukin (IL)-1 cytokine family - balance between agonists and antagonists in inflammatory diseases. Cytokine. 2015. 76: 25–37.
5. Masters, S. L., Simon, A., Aksentijevich, I., and Kastner, D. L., Horror autoinflammaticus: the molecular pathophysiology of autoinflammatory disease. Annu. Rev. Immunol. 2009. 27: 621–668.
6. Martinon, F., Pétrilli, V., Mayor, A., Tardivel, A., and Tschopp, J., Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature. 2006. 440: 237–241.
7. Aksentijevich, I., Nowak, M., Mustapha, M., and Chae, J. J., De Novo CIAS1 mutations, cytokine activation, and evidence for genetic heterogeneity in patients with Neonatal-Onset Multisystem Inflammatory Disease (NOMID). 2015. 57: 742–768.
8. Dinarello, C. A. and van der Meer, J. W. M., Treating inflammation by blocking interleukin-1 in humans. Semin. Immunol. 2013. 25: 469–484.
9. Ridker, P. M. and Lüscher, T. F., Anti-inflammatory therapies for cardiovascular disease. Eur. Heart J. 2014. 35: 1782–1791.
10. Ridker, P. M., Everett, B. M., Thuren, T., MacFadyen, J. G., Chang, W. H., Ballantyne, C., Fonseca, F. et al., Antiinflammatory therapy with canakinumab for atherosclerotic disease. N. Engl. J. Med. 2017. NEJMoa1707914. 377: 1119–1131
11. Dinarello, C. A., Interleukin-18 and the pathogenesis of inflammatory diseases. Semin. Nephrol. 2007. 27: 98–114.
12. Rubartelli, A., Cozzolino, F., Talio, M. and Sitia, R., A novel secretory pathway for interleukin-1 beta, a protein lacking a signal sequence. EMBO J. 1990. 9: 1503–1510.
13. Keller, M., Rüegg, A., Werner, S. and Beer, H. D., Active caspase-1 is a regulator of unconventional protein secretion. Cell. 2008. 132: 818–831.
14. Brough, D., and Rothwell, N. J., Caspase-1-dependent processing of pro-interleukin-1beta is cytosolic and precedes cell death. J. Cell Sci. 2007. 120: 772–781.
15. Yannik, H., Luciani, M., Becq, F., Verrier, B. and Rubartelli, A. C. G., Interleukin-1b secretion is impaired by inhibitors of the Atp binding cassette transporter, ABC1. Blood. 1997. 90: 2911–2915.
16. Zhou, X., Engel, T., Goepfert, C., Erren, M., Assmann, G. and von Eckardstein, A., The ATP binding cassette transporter A1 contributes to the secretion of interleukin 1β from macrophages but not from monocytes. Biochem. Biophys. Res. Commun. 2002. 291: 598–604.
17. Shirasaki, Y., Yamagishi, M., Suzuki, N., Izawa, K., Nakahara, A., Mizuno, J., Shoji, S. et al., Real-time single-cell imaging of protein secretion. Sci. Rep. 2015. 4: 4736.
18. Martín-sánchez, F., Diamond, C., Zeitler, M., Gomez-sanchez, A., Peñalver, M., Paszek, P., Steringer, J. P. et al., Inflammasome-dependent IL-1 β release depends upon membrane permeabilisation. Cell Death Differ. 2016. 23: 1219–1231.
19. Andrei, C., Dazzi, C., Lotti, L., Torrisi, M. R., Chimini, G. and Rubartelli, A., The secretory route of the leaderless protein interleukin 1beta involves exocytosis of endolysosome-related vesicles. Mol. Biol Cell. 1999. 10: 1463–1475.
20. MacKenzie, A., Wilson, H. L., Kiss-Toth, E., Dower, S. K., North, R. A. and Surprenant, A., Rapid secretion of interleukin-1β by microvesicle shedding. Immunity. 2001. 15: 825–835.
21. Zhang, M., Kenny, S. J., Ge, L., Xu, K. and Schekman, R., Translocation of interleukin-1β into a vesicle intermediate in autophagy- mediated secretion. Elife. 2015. 4: 1–23.
22. Andrei, C., Margiocco, P., Poggi, A., Lotti, L. V., Torrisi, M. R. and Rubartelli, A., Phospholipases C and A2 control lysosome-mediated IL-1 beta secretion: Implications for inflammatory processes. Proc. Natl. Acad. Sci. USA. 2004. 101: 9745–9750.
23. Thornberry, N.A1., Bull, H. G., Calaycay, J. R., Chapman, K. T., Howard, A. D., Kostura, M. J., Miller, D. K. et al., A novel heterodimeric cysteine protease is required for interleukin-1b processing in monocytes. Nature 1992. 355: 472–475.
24. Ghayur, T., Banerjee, S., Hugunin, M., Butler, D., Herzog, L., Carter, A., Quintal, L. et al., Caspase-1 processes IFNg-inducing factor and regulates LPS-induced IFNg production. Nature. 1997. 386: 619–623.
25. Kostura, M. J., Tocci, M. J., Limjuco, G., Chin, J., Cameron, P., Hillman, A. G., Chartrain, N. A. et al., Identification of a monocyte specific pre-interleukin 1i8 convertase activity. 2000. 86: 5227–5231.
26. Broz, P. and Dixit, V. M., Inflammasomes: mechanism of assembly, regulation and signalling. Nat. Rev. Immunol. 2016. 16: 407–420.
27. Kayagaki, N., Warming, S., Lamkanfi, M., Vande, W. L., Louie, S., Dong, J., Newton, K. et al., Non-canonical inflammasome activation targets caspase-11. Nature. 2011. 479: 117–121.
28. Shi, J., Zhao, Y., Wang, K., Shi, X., Wang, Y., Huang, H., Zhuang, Y. et al., Cleavage of GSDMD by inflammatory caspases determines pyroptotic cell death. Nature 2015. 526: 660–665.
29. Aglietti, R. A., Estevez, A., Gupta, A., Ramirez, M. G., Liu, P. S., Kayagaki, N., Ciferri, C. et al., GsdmD p30 elicited by caspase-11 during pyroptosis forms pores in membranes. Proc. Natl. Acad. Sci. 2016. 113: 7858–7863.
30. Ding, J., Wang, K., Liu, W., She, Y., Sun, Q., Shi, J., Sun, H. et al., Pore-forming activity and structural autoinhibition of the gasdermin family. Nature. 2016. 535: 111–116.
31. Sborgi, L., Rühl, S., Mulvihill, E., Pipercevic, J., Heilig, R., Stahlberg, H., Farady, C. et al., GSDMD membrane pore formation constitutes the mechanism of pyroptotic cell death. EMBO J. 2016. 35: e201694696-13.
32. Liu, X., Zhang, Z., Ruan, J., Pan, Y., Magupalli, V. G., Wu, H. and Lieberman, J., Inflammasome-activated gasdermin D causes pyroptosis by forming membrane pores. Nature. 2016. 535: 153–158.
33. He, W., Wan, H., Hu, L., Chen, P., Wang, X., Huang, Z., Yang, Z.-H. et al., Gasdermin D is an executor of pyroptosis and required for interleukin-1β secretion. Cell Res. 2015. 25: 1285–1298.
34. Fink, S. L. and Cookson, B. T., Caspase-1-dependent pore formation during pyroptosis leads to osmotic lysis of infected host macrophages. Cell. Microbiol. 2006. 8:1812–1825.
35. Verhoef, P. A., Kertesy, S. B., Estacion, M., Schilling, W. P. and Dubyak, G. R., Maitotoxin induces biphasic interleukin-1beta secretion and membrane blebbing in murine macrophages. Mol. Pharmacol. 2004. 66: 909–920.
36. Schemmer, P. and Bradford, B. U., Rose ML, Bunzendahl H, Raleigh JA., and Lemasters JJ. TRG. Intravenous glycine improves survival in rat liver transplantation. Am. J. Physiol. 1999. 276: G924-G932.
37. Kayagaki, N., Stowe, I. B., Lee, B. L., O'Rourke, K., Anderson, K., Warming, S., Cuellar, T. et al., Caspase-11 cleaves gasdermin D for non-canonical inflammasome signalling. Nature. 2015. 526: 666–671.
38. Rogers, C., Fernandes-Alnemri, T., Mayes, L., Alnemri, D., Cingolani, G. and Alnemri, E. S., Cleavage of DFNA5 by caspase-3 during apoptosis mediates progression to secondary necrotic/pyroptotic cell death. Nat. Commun. 2017. 8: 14128.
39. Wang, Y., Gao, W., Shi, X., Ding, J., Liu, W., He, H., Wang, K. et al., Chemotherapy drugs induce pyroptosis through caspase-3 cleavage of a gasdermin. Nature. 2017. 547: 99–103.
40. Zanoni, I., Tan, Y., Di Gioia, M., Broggi, A., Ruan, J., Shi, J., Donado, C. A. et al., An endogenous caspase-11 ligand elicits interleukin-1 release from living dendritic cells. Science (80-.). 2016. 352: 1232–1236.
41. Chen, K. W., Groß, C. J., Sotomayor, F., Stacey, K. J., Tschopp, J., Sweet, M. J. and Schroder, K., The neutrophil NLRC4 inflammasome selectively promotes IL-1b maturation without pyroptosis during acute salmonella challenge. Cell Rep. 2014. 8: 570–582.
42. Karmakar, M., Katsnelson, M. A., Dubyak, G. R. and Pearlman, E., Neutrophil P2X7 receptors mediate NLRP3 inflammasome-dependent IL-1β secretion in response to ATP. Nat. Commun. 2016. 7: 10555.
43. Monteleone, M., Stow, J. L. and Schroder, K., Mechanisms of unconventional secretion of IL-1 family cytokines. Cytokine. 2015. 74: 213–218.
44. Martín-Sánchez, F., Diamond, C., Zeitler, M., Gomez-Sanchez, A., Peñalver, M., Paszek, P., Steringer, J. P. et al., Inflammasome-dependent IL-1 β release depends upon membrane permeabilisation. Cell Death Differ. 2016. 23: 1219–1231.
45. Conos, S. A., Lawlor, K. E., Vaux, D. L., Vince, J. E. and Lindqvist, L. M., Cell death is not essential for caspase-1-mediated interleukin-1β activation and secretion. Cell Death Differ. 2016. 23: 1827–1838.
46. Gong, Y. N., Guy, C., Olauson, H., Becker, J. U., Yang, M., Fitzgerald, P., Linkermann, A. et al., ESCRT-III acts downstream of MLKL to regulate necroptotic cell death and its consequences. Cell. 2017. 169: 286–300.e16.
47. Anggayasti, W. L., Mancera, R. L., Bottomley, S. and Helmerhorst, E., The self-association of HMGB1 and its possible role in the binding to DNA and cell membrane receptors. FEBS Lett. 2017. 591: 282–294.
48. Duguet, M. and de Recondo AM. A deoxyribonucleic acid unwinding protein isolated from regenerating rat liver. Physical and functional properties. J. Biol. Chem. 1978. 253: 1660–1666.
49. Watson, M., Stott, K., Fischl, H., Cato, L. and Thomas, J. O., Characterization of the interaction between HMGB1 and H3-a possible means of positioning HMGB1 in chromatin. Nucleic Acids Res. 2014. 42: 848–859.
50. Lotze, M. T. and Tracey, K. J., High-mobility group box 1 protein (HMGB1): nuclear weapon in the immune arsenal. Nat. Rev. Immunol. 2005. 5: 331–342.
51. Miao, E. A., Leaf, I. A., Treuting, P. M., Mao, D. P., Dors, M., Sarkar, A., Warren, S. E. et al., Caspase-1-induced pyroptosis is an innate immune effector mechanism against intracellular bacteria. Nat. Immunol. 2010. 11: 1136–1142.
52. Broz, P., Von Moltke, J., Jones, J. W., Vance, R. E. and Monack, D. M., Differential requirement for caspase-1 autoproteolysis in pathogen-induced cell death and cytokine processing. Cell Host Microbe. 2010. 8: 471–483.
53. Gross, O., Measuring the Inflammasome. Methods Mol. Biol. Springer. 2012. 844: 199–222.