Structural insights into cytokine cleavage by inflammatory caspase-4.
Journal
Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462
Informations de publication
Date de publication:
Dec 2023
Dec 2023
Historique:
received:
17
05
2023
accepted:
16
10
2023
pubmed:
23
11
2023
medline:
23
11
2023
entrez:
22
11
2023
Statut:
ppublish
Résumé
Inflammatory caspases are key enzymes in mammalian innate immunity that control the processing and release of interleukin-1 (IL-1)-family cytokines
Identifiants
pubmed: 37993712
doi: 10.1038/s41586-023-06751-9
pii: 10.1038/s41586-023-06751-9
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
451-459Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Nature Limited.
Références
Dinarello, C. A. Overview of the IL-1 family in innate inflammation and acquired immunity. Immunol. Rev. 281, 8–27 (2018).
pubmed: 29247995
pmcid: 5756628
doi: 10.1111/imr.12621
Bateman, G., Hill, B., Knight, R. & Boucher, D. Great balls of fire: activation and signalling of inflammatory caspases. Biochem. Soc. Trans. 49, 1311–1324 (2021).
pubmed: 34060593
pmcid: 8286819
doi: 10.1042/BST20200986
Chan, A. H. & Schroder, K. Inflammasome signaling and regulation of interleukin-1 family cytokines. J. Exp. Med. 217, e20190314 (2020).
pubmed: 31611248
doi: 10.1084/jem.20190314
Shi, J. et al. Cleavage of GSDMD by inflammatory caspases determines pyroptotic cell death. Nature 526, 660–665 (2015).
pubmed: 26375003
doi: 10.1038/nature15514
Kayagaki, N. et al. Caspase-11 cleaves gasdermin D for non-canonical inflammasome signalling. Nature 526, 666–671 (2015).
pubmed: 26375259
doi: 10.1038/nature15541
Julien, O. & Wells, J. A. Caspases and their substrates. Cell Death Differ. 24, 1380–1389 (2017).
pubmed: 28498362
pmcid: 5520456
doi: 10.1038/cdd.2017.44
Wang, K. et al. Structural mechanism for GSDMD targeting by autoprocessed caspases in pyroptosis. Cell 180, 941–955 (2020).
pubmed: 32109412
doi: 10.1016/j.cell.2020.02.002
Liu, Z. et al. Caspase-1 engages full-length gasdermin D through two distinct interfaces that mediate caspase recruitment and substrate cleavage. Immunity 53, 106–114 (2020).
pubmed: 32553275
pmcid: 7382298
doi: 10.1016/j.immuni.2020.06.007
Shi, J., Gao, W. & Shao, F. Pyroptosis: gasdermin-mediated programmed necrotic cell death. Trends Biochem. Sci. 42, 245–254 (2017).
pubmed: 27932073
doi: 10.1016/j.tibs.2016.10.004
Evavold, C. L. et al. The pore-forming protein gasdermin D regulates interleukin-1 secretion from living macrophages. Immunity 48, 35–44 (2018).
pubmed: 29195811
doi: 10.1016/j.immuni.2017.11.013
Heilig, R. et al. The gasdermin-D pore acts as a conduit for IL-1β secretion in mice. Eur. J. Immunol. 48, 584–592 (2018).
pubmed: 29274245
doi: 10.1002/eji.201747404
Xia, S. et al. Gasdermin D pore structure reveals preferential release of mature interleukin-1. Nature 593, 607–611 (2021).
pubmed: 33883744
pmcid: 8588876
doi: 10.1038/s41586-021-03478-3
Barnett, K. C., Li, S., Liang, K. & Ting, J. P.-Y. A 360° view of the inflammasome: mechanisms of activation, cell death, and diseases. Cell 186, 2288–2312 (2023).
pubmed: 37236155
doi: 10.1016/j.cell.2023.04.025
Kagan, J. C., Magupalli, V. G. & Wu, H. SMOCs: supramolecular organizing centres that control innate immunity. Nat. Rev. Immunol. 14, 821–826 (2014).
pubmed: 25359439
pmcid: 4373346
doi: 10.1038/nri3757
Thornberry, N. A. et al. A novel heterodimeric cysteine protease is required for interleukin-1 β processing in monocytes. Nature 356, 768–774 (1992).
pubmed: 1574116
doi: 10.1038/356768a0
Devant, P., Cao, A. & Kagan, J. C. Evolution-inspired redesign of the LPS receptor caspase-4 into an interleukin-1β–converting enzyme. Sci. Immunol. 6, eabh3567 (2021).
pubmed: 34734155
pmcid: 8559778
doi: 10.1126/sciimmunol.abh3567
Bibo-Verdugo, B., Snipas, S. J., Kolt, S., Poreba, M. & Salvesen, G. S. Extended subsite profiling of the pyroptosis effector protein gasdermin D reveals a region recognized by inflammatory caspase-11. J. Biol. Chem. 295, 11292–11302 (2020).
Faucheu, C. et al. A novel human protease similar to the interleukin-1 beta converting enzyme induces apoptosis in transfected cells. EMBO J. 14, 1914–1922 (1995).
pubmed: 7743998
pmcid: 398290
doi: 10.1002/j.1460-2075.1995.tb07183.x
Kamens, J. et al. Identification and characterization of ICH-2, a novel member of the interleukin-1β-converting enzyme family of cysteine proteases. J. Biol. Chem. 270, 15250–15256 (1995).
pubmed: 7797510
doi: 10.1074/jbc.270.25.15250
Shi, J. et al. Inflammatory caspases are innate immune receptors for intracellular LPS. Nature 514, 187–192 (2014).
pubmed: 25119034
doi: 10.1038/nature13683
Rühl, S. & Broz, P. Caspase-11 activates a canonical NLRP3 inflammasome by promoting K
pubmed: 26173909
doi: 10.1002/eji.201545772
Baker, P. J. et al. NLRP3 inflammasome activation downstream of cytoplasmic LPS recognition by both caspase-4 and caspase-5. Eur. J. Immunol. 45, 2918–2926 (2015).
pubmed: 26173988
doi: 10.1002/eji.201545655
Kayagaki, N. et al. Non-canonical inflammasome activation targets caspase-11. Nature 479, 117–121 (2011).
pubmed: 22002608
doi: 10.1038/nature10558
Wandel, M. P. et al. Guanylate-binding proteins convert cytosolic bacteria into caspase-4 signaling platforms. Nat. Immunol. 21, 880–891 (2020).
Knodler, L. A. et al. Noncanonical inflammasome activation of caspase-4/caspase-11 mediates epithelial defenses against enteric bacterial pathogens. Cell Host Microbe 16, 249–256 (2014).
pubmed: 25121752
pmcid: 4157630
doi: 10.1016/j.chom.2014.07.002
Devant, P. & Kagan, J. C. Protocol to purify recombinant inflammatory caspases and assess their catalytic activity in vitro. STAR Protoc. 3, 101848 (2022).
pubmed: 36595884
pmcid: 9668568
doi: 10.1016/j.xpro.2022.101848
Holly, M. K. et al. Salmonella enterica infection of murine and human enteroid-derived monolayers elicits differential activation of epithelium-intrinsic inflammasomes. Infect. Immun. 88, e00017-20 (2020).
pubmed: 32284374
pmcid: 7309616
doi: 10.1128/IAI.00017-20
Naseer, N. et al. Salmonella enterica Serovar Typhimurium induces NAIP/NLRC4- and NLRP3/ASC-independent, caspase-4-dependent inflammasome activation in human intestinal epithelial cells. Infect. Immun. 90, e0066321 (2022).
pubmed: 35678562
doi: 10.1128/iai.00663-21
Kobayashi, T. et al. The Shigella OspC3 effector inhibits caspase-4, antagonizes inflammatory cell death, and promotes epithelial infection. Cell Host Microbe 13, 570–583 (2013).
pubmed: 23684308
doi: 10.1016/j.chom.2013.04.012
Gritsenko, A. et al. Priming is dispensable for NLRP3 inflammasome activation in human monocytes in vitro. Front. Immunol. 11, 565924 (2020).
pubmed: 33101286
pmcid: 7555430
doi: 10.3389/fimmu.2020.565924
Coll, R. C. et al. A small-molecule inhibitor of the NLRP3 inflammasome for the treatment of inflammatory diseases. Nat. Med. 21, 248–255 (2015).
pubmed: 25686105
pmcid: 4392179
doi: 10.1038/nm.3806
Reyes Ruiz, V. M. et al. Broad detection of bacterial type III secretion system and flagellin proteins by the human NAIP/NLRC4 inflammasome. Proc. Natl Acad. Sci. USA 114, 13242–13247 (2017).
pubmed: 29180436
pmcid: 5740664
doi: 10.1073/pnas.1710433114
Tsutsumi, N. et al. The structural basis for receptor recognition of human interleukin-18. Nat. Commun. 5, 5340 (2014).
pubmed: 25500532
doi: 10.1038/ncomms6340
Krissinel, E. & Henrick, K. Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774–797 (2007).
pubmed: 17681537
doi: 10.1016/j.jmb.2007.05.022
Jumper, J. et al. Highly accurate protein structure prediction with AlphaFold. Nature 596, 583–589 (2021).
pubmed: 34265844
pmcid: 8371605
doi: 10.1038/s41586-021-03819-2
Evavold, C. L. et al. Control of gasdermin D oligomerization and pyroptosis by the Ragulator–Rag–mTORC1 pathway. Cell 184, 4495–4511 (2021).
pubmed: 34289345
pmcid: 8380731
doi: 10.1016/j.cell.2021.06.028
Roschitzki-Voser, H. et al. Human caspases in vitro: expression, purification and kinetic characterization. Protein Expr. Purif. 84, 236–246 (2012).
pubmed: 22683476
doi: 10.1016/j.pep.2012.05.009
Hu, J. J. et al. FDA-approved disulfiram inhibits pyroptosis by blocking gasdermin D pore formation. Nat. Immunol. 21, 736–745 (2020).
pubmed: 32367036
pmcid: 7316630
doi: 10.1038/s41590-020-0669-6
Mastronarde, D. N. Automated electron microscope tomography using robust prediction of specimen movements. J. Struct. Biol. 152, 36–51 (2005).
pubmed: 16182563
doi: 10.1016/j.jsb.2005.07.007
Morin, A. et al. Collaboration gets the most out of software. eLife 2, e01456 (2013).
pubmed: 24040512
pmcid: 3771563
doi: 10.7554/eLife.01456
Zheng, S. Q. et al. MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy. Nat. Methods 14, 331–332 (2017).
pubmed: 28250466
pmcid: 5494038
doi: 10.1038/nmeth.4193
Punjani, A., Rubinstein, J. L., Fleet, D. J. & Brubaker, M. A. cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination. Nat. Methods 14, 290–296 (2017).
pubmed: 28165473
doi: 10.1038/nmeth.4169
Klaholz, B. P. Deriving and refining atomic models in crystallography and cryo-EM: the latest Phenix tools to facilitate structure analysis. Acta Crystallogr. D 75, 878–881 (2019).
doi: 10.1107/S2059798319013391
Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D 66, 213–221 (2010).
pubmed: 20124702
pmcid: 2815670
doi: 10.1107/S0907444909052925
Goddard, T. D. et al. UCSF ChimeraX: meeting modern challenges in visualization and analysis. Protein Sci. 27, 14–25 (2018).
pubmed: 28710774
doi: 10.1002/pro.3235
Mirdita, M. et al. ColabFold: making protein folding accessible to all. Nat. Methods 19, 679–682 (2022).
pubmed: 35637307
pmcid: 9184281
doi: 10.1038/s41592-022-01488-1
Mintseris, J. & Gygi, S. P. High-density chemical cross-linking for modeling protein interactions. Proc. Natl Acad. Sci. USA 117, 93–102 (2020).
pubmed: 31848235
doi: 10.1073/pnas.1902931116
Wynosky-Dolfi, M. A. et al. Oxidative metabolism enables Salmonella evasion of the NLRP3 inflammasome. J. Exp. Med. 211, 653–668 (2014).
pubmed: 24638169
pmcid: 3978275
doi: 10.1084/jem.20130627