GSDMD membrane pore formation constitutes the mechanism of pyroptotic cell death

EMBO Journal

Volumn 35, Issue 16, 2016, Pages 1766-1778

  Sborgi, Lorenzo ^a   Rühl, Sebastian ^a   Mulvihill, Estefania ^b   Pipercevic, Joka ^a   Heilig, Rosalie ^a   Stahlberg, Henning ^a   Farady, Christopher J ^c   Müller, Daniel J ^b   Broz, Petr ^a   Hiller, Sebastian ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b ETH ZURICH   (Switzerland)

^c NOVARTIS PHARMA AG   (Switzerland)

Author keywords

atomic force microscopy; cell death; gasdermin; inflammasomes; inflammation; pyroptosis

Indexed keywords

GASDERMIN D; INTERLEUKIN 1BETA CONVERTING ENZYME; LIPOSOME; PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; ATOMIC FORCE MICROSCOPY; CELL MEMBRANE; CHANNEL GATING; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; HUMAN; HUMAN CELL; IN VITRO STUDY; MACROPHAGE; MOLECULAR MECHANICS; PRIORITY JOURNAL; PROTEIN BINDING; PYROPTOSIS; SIGNAL TRANSDUCTION;

EID: 84982102736     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201694696     Document Type: Article

References (45)

1. Aglietti RA, Estevez A, Gupta A, Ramirez MG, Liu PS, Kayagaki N, Ciferri C, Dixit VM, Dueber EC (2016) GsdmD p30 elicited by caspase-11 during pyroptosis forms pores in membranes. Proc Natl Acad Sci USA 113: 7858–7963
2. Bergsbaken T, Fink SL, Cookson BT (2009) Pyroptosis: host cell death and inflammation. Nat Rev Microbiol 7: 99–109
3. Broz P, Ruby T, Belhocine K, Bouley DM, Kayagaki N, Dixit VM, Monack DM (2012) Caspase-11 increases susceptibility to Salmonella infection in the absence of caspase-1. Nature 490: 288–291
4. Broz P (2015) Immunology: caspase target drives pyroptosis. Nature 526: 642–643
5. Cai Z, Jitkaew S, Zhao J, Chiang HC, Choksi S, Liu J, Ward Y, Wu LG, Liu ZG (2014) Plasma membrane translocation of trimerized MLKL protein is required for TNF-induced necroptosis. Nat Cell Biol 16: 55–65
6. Chen X, Li W, Ren J, Huang D, He WT, Song Y, Yang C, Li W, Zheng X, Chen P, Han J (2014) Translocation of mixed lineage kinase domain-like protein to plasma membrane leads to necrotic cell death. Cell Res 24: 105–121
7. Czabotar PE, Westphal D, Dewson G, Ma S, Hockings C, Fairlie WD, Lee EF, Yao S, Robin AY, Smith BJ, Huang DC, Kluck RM, Adams JM, Colman PM (2013) Bax crystal structures reveal how BH3 domains activate Bax and nucleate its oligomerization to induce apoptosis. Cell 152: 519–531
8. Dick MS, Sborgi L, Ruhl S, Hiller S, Broz P (2016) ASC filament formation serves as a signal amplification mechanism for inflammasomes. Nat Commun 7: 11929
9. Ding J, Wang K, Liu W, She Y, Sun Q, Shi J, Sun H, Wang DC, Shao F (2016) Pore-forming activity and structural autoinhibition of the gasdermin family. Nature 535: 111–116
10. Dondelinger Y, Declercq W, Montessuit S, Roelandt R, Goncalves A, Bruggeman I, Hulpiau P, Weber K, Sehon CA, Marquis RW, Bertin J, Gough PJ, Savvides S, Martinou JC, Bertrand MJ, Vandenabeele P (2014) MLKL compromises plasma membrane integrity by binding to phosphatidylinositol phosphates. Cell Rep 7: 971–981
11. Dufrene YF, Martinez-Martin D, Medalsy I, Alsteens D, Muller DJ (2013) Multiparametric imaging of biological systems by force-distance curve-based AFM. Nat Methods 10: 847–854
12. Fink SL, Cookson BT (2007) Pyroptosis and host cell death responses during Salmonella infection. Cell Microbiol 9: 2562–2570
13. Fink SL, Bergsbaken T, Cookson BT (2008) Anthrax lethal toxin and Salmonella elicit the common cell death pathway of caspase-1-dependent pyroptosis via distinct mechanisms. Proc Natl Acad Sci USA 105: 4312–4317
14. Gatfield J, Pieters J (2000) Essential role for cholesterol in entry of mycobacteria into macrophages. Science 288: 1647–1650
15. Gavathiotis E, Suzuki M, Davis ML, Pitter K, Bird GH, Katz SG, Tu HC, Kim H, Cheng EH, Tjandra N, Walensky LD (2008) BAX activation is initiated at a novel interaction site. Nature 455: 1076–1081
16. Hagar JA, Powell DA, Aachoui Y, Ernst RK, Miao EA (2013) Cytoplasmic LPS activates caspase-11: implications in TLR4-independent endotoxic shock. Science 341: 1250–1253
17. He WT, Wan H, Hu L, Chen P, Wang X, Huang Z, Yang ZH, Zhong CQ, Han J (2015) Gasdermin D is an executor of pyroptosis and required for interleukin-1beta secretion. Cell Res 25: 1285–1298
18. Kayagaki N, Warming S, Lamkanfi M, Vande Walle L, Louie S, Dong J, Newton K, Qu Y, Liu J, Heldens S, Zhang J, Lee WP, Roose-Girma M, Dixit VM (2011) Non-canonical inflammasome activation targets caspase-11. Nature 479: 117–121
19. Kayagaki N, Wong MT, Stowe IB, Ramani SR, Gonzalez LC, Akashi-Takamura S, Miyake K, Zhang J, Lee WP, Muszynski A, Forsberg LS, Carlson RW, Dixit VM (2013) Noncanonical inflammasome activation by intracellular LPS independent of TLR4. Science 341: 1246–1249
20. Kayagaki N, Stowe IB, Lee BL, O'Rourke K, Anderson K, Warming S, Cuellar T, Haley B, Roose-Girma M, Phung QT, Liu PS, Lill JR, Li H, Wu J, Kummerfeld S, Zhang J, Lee WP, Snipas SJ, Salvesen GS, Morris LX et al (2015) Caspase-11 cleaves gasdermin D for non-canonical inflammasome signalling. Nature 526: 666–671
21. Lamkanfi M (2011) Emerging inflammasome effector mechanisms. Nat Rev Immunol 11: 213–220
22. Latz E, Xiao TS, Stutz A (2013) Activation and regulation of the inflammasomes. Nat Rev Immunol 13: 397–411
23. Leung C, Dudkina NV, Lukoyanova N, Hodel AW, Farabella I, Pandurangan AP, Jahan N, Pires Damaso M, Osmanovic D, Reboul CF, Dunstone MA, Andrew PW, Lonnen R, Topf M, Saibil HR, Hoogenboom BW (2014) Stepwise visualization of membrane pore formation by suilysin, a bacterial cholesterol-dependent cytolysin. elife 3: e04247
24. Mariathasan S, Newton K, Monack DM, Vucic D, French DM, Lee WP, Roose-Girma M, Erickson S, Dixit VM (2004) Differential activation of the inflammasome by caspase-1 adaptors ASC and Ipaf. Nature 430: 213–218
25. Miao EA, Leaf IA, Treuting PM, Mao DP, Dors M, Sarkar A, Warren SE, Wewers MD, Aderem A (2010) Caspase-1-induced pyroptosis is an innate immune effector mechanism against intracellular bacteria. Nat Immunol 11: 1136–1142
26. von Moltke J, Ayres JS, Kofoed EM, Chavarria-Smith J, Vance RE (2013) Recognition of bacteria by inflammasomes. Annu Rev Immunol 31: 73–106
27. Muller DJ, Amrein M, Engel A (1997) Adsorption of biological molecules to a solid support for scanning probe microscopy. J Struct Biol 119: 172–188
28. Mulvihill E, van Pee K, Mari SA, Muller DJ, Yildiz O (2015) Directly Observing the Lipid-Dependent Self-Assembly and Pore-Forming Mechanism of the Cytolytic Toxin Listeriolysin O. Nano Lett 15: 6965–6973
29. Murphy JM, Czabotar PE, Hildebrand JM, Lucet IS, Zhang JG, Alvarez-Diaz S, Lewis R, Lalaoui N, Metcalf D, Webb AI, Young SN, Varghese LN, Tannahill GM, Hatchell EC, Majewski IJ, Okamoto T, Dobson RC, Hilton DJ, Babon JJ, Nicola NA et al (2013) The pseudokinase MLKL mediates necroptosis via a molecular switch mechanism. Immunity 39: 443–453
30. Op de Beeck K, Van Camp G, Thys S, Cools N, Callebaut I, Vrijens K, Van Nassauw L, Van Tendeloo VF, Timmermans JP, Van Laer L (2011) The DFNA5 gene, responsible for hearing loss and involved in cancer, encodes a novel apoptosis-inducing protein. Eur J Hum Genet 19: 965–973
31. Pasparakis M, Vandenabeele P (2015) Necroptosis and its role in inflammation. Nature 517: 311–320
32. Pfreundschuh M, Martinez-Martin D, Mulvihill E, Wegmann S, Muller DJ (2014) Multiparametric high-resolution imaging of native proteins by force-distance curve-based AFM. Nat Protoc 9: 1113–1130
33. Podobnik M, Marchioretto M, Zanetti M, Bavdek A, Kisovec M, Cajnko MM, Lunelli L, Dalla Serra M, Anderluh G (2015) Plasticity of listeriolysin O pores and its regulation by pH and unique histidine. Sci Rep 5: 9623
34. Ramage P, Cheneval D, Chvei M, Graff P, Hemmig R, Heng R, Kocher HP, Mackenzie A, Memmert K, Revesz L, Wishart W (1995) Expression, refolding, and autocatalytic proteolytic processing of the interleukin-1 beta-converting enzyme precursor. J Biol Chem 270: 9378–9383
35. Saeki N, Kim DH, Usui T, Aoyagi K, Tatsuta T, Aoki K, Yanagihara K, Tamura M, Mizushima H, Sakamoto H, Ogawa K, Ohki M, Shiroishi T, Yoshida T, Sasaki H (2007) GASDERMIN, suppressed frequently in gastric cancer, is a target of LMO1 in TGF-beta-dependent apoptotic signalling. Oncogene 26: 6488–6498
36. Scherrer R, Gerhardt P (1971) Molecular sieving by the Bacillus megaterium cell wall and protoplast. J Bacteriol 107: 718–735
37. Shi J, Zhao Y, Wang Y, Gao W, Ding J, Li P, Hu L, Shao F (2014) Inflammatory caspases are innate immune receptors for intracellular LPS. Nature 514: 187–192
38. Shi J, Zhao Y, Wang K, Shi X, Wang Y, Huang H, Zhuang Y, Cai T, Wang F, Shao F (2015) Cleavage of GSDMD by inflammatory caspases determines pyroptotic cell death. Nature 526: 660–665
39. Sonnen AF, Plitzko JM, Gilbert RJ (2014) Incomplete pneumolysin oligomers form membrane pores. Open Biol 4: 140044
40. Su L, Quade B, Wang H, Sun L, Wang X, Rizo J (2014) A plug release mechanism for membrane permeation by MLKL. Structure 22: 1489–1500
41. Suzuki M, Youle RJ, Tjandra N (2000) Structure of Bax: coregulation of dimer formation and intracellular localization. Cell 103: 645–654
42. Tanaka S, Mizushina Y, Kato Y, Tamura M, Shiroishi T (2013) Functional conservation of Gsdma cluster genes specifically duplicated in the mouse genome. G3 (Bethesda) 3: 1843–1850
43. Thornberry NA, Bull HG, Calaycay JR, Chapman KT, Howard AD, Kostura MJ, Miller DK, Molineaux SM, Weidner JR, Aunins J, Elliston KO, Ayala JM, Casano FJ, Chin J, Ding GJF, Egger LA, Gaffney EP, Limjuco G, Palyha OC, Raju SM et al (1992) A novel heterodimeric cysteine protease is required for interleukin-1 beta processing in monocytes. Nature 356: 768–774
44. Wang H, Sun L, Su L, Rizo J, Liu L, Wang LF, Wang FS, Wang X (2014) Mixed lineage kinase domain-like protein MLKL causes necrotic membrane disruption upon phosphorylation by RIP3. Mol Cell 54: 133–146
45. Youle RJ, Strasser A (2008) The BCL-2 protein family: opposing activities that mediate cell death. Nat Rev Mol Cell Biol 9: 47–59