Lipid-protein interactions regulating the canonical and the non-canonical NLRP3 inflammasome

Progress in Lipid Research - Tập 87 - Trang 101182 - 2022
Malvina Pizzuto1,2, Pablo Pelegrin1,3, Jean-Marie Ruysschaert2
1Molecular Inflammation Group, Biomedical Research Institute of Murcia (IMIB), Murcia, Spain
2Laboratoire de Structure et Fonction des Membranes Biologiques, Université Libre de Bruxelles, Brussels, Belgium
3Department of Biochemistry and Molecular Biology B and Immunology, Faculty of Biology, University of Murcia, Spain

Tài liệu tham khảo

Mariathasan, 2006, Cryopyrin activates the inflammasome in response to toxins and ATP, Nature, 440, 228, 10.1038/nature04515 Mayor, 2006, Gout-associated uric acid crystals activate the NALP3 inflammasome, Nature, 440, 237, 10.1038/nature04516 Duewell, 2010, NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals, Nature, 464, 1357, 10.1038/nature08938 Hornung, 2008, Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization, Nat. Immunol., 9, 847, 10.1038/ni.1631 Heneka, 2013, NLRP3 is activated in Alzheimer’s disease and contributes to pathology in APP/PS1 mice, Nature, 493, 674, 10.1038/nature11729 Patel, 2017, Inflammasome priming in sterile inflammatory disease, Trends Mol. Med., 23, 165, 10.1016/j.molmed.2016.12.007 Baker, 2017, Posttranslational modification as a critical determinant of cytoplasmic innate immune recognition, Physiol. Rev., 97, 1165, 10.1152/physrev.00026.2016 Andreeva, 2021, NLRP3 cages revealed by full-length mouse NLRP3 structure control pathway activation, Cell, 184, 6299, 10.1016/j.cell.2021.11.011 Hochheiser, 2022, Structure of the NLRP3 decamer bound to the cytokine release inhibitor CRID3, Nature, 604, 184, 10.1038/s41586-022-04467-w Ohto, 2007, Crystal structures of human MD-2 and its complex with antiendotoxic lipid IVa, Science, 316, 1632, 10.1126/science.1139111 Martín-Sánchez, 2017, Lytic cell death induced by melittin bypasses pyroptosis but induces NLRP3 inflammasome activation and IL-1β release, Cell Death Dis., 8, e2984, 10.1038/cddis.2017.390 Tapia-Abellán, 2021, Sensing low intracellular potassium by NLRP3 results in a stable open structure that promotes inflammasome activation, Sci. Adv., 7, 10.1126/sciadv.abf4468 Di, 2018, The TWIK2 potassium Efflux Channel in macrophages mediates NLRP3 Inflammasome-induced inflammation, Immunity, 49, 56, 10.1016/j.immuni.2018.04.032 Pelegrin, 2021, P2X7 receptor and the NLRP3 inflammasome: partners in crime, Biochem. Pharmacol., 187, 10.1016/j.bcp.2020.114385 Muñoz-Planillo, 2013, K+ efflux is the common trigger of NLRP3 Inflammasome activation by bacterial toxins and particulate matter, Immunity, 38, 1142, 10.1016/j.immuni.2013.05.016 Groß, 2016, K + efflux-independent NLRP3 Inflammasome activation by small molecules targeting mitochondria, Immunity, 45, 761, 10.1016/j.immuni.2016.08.010 Chen, 2018, PtdIns4P on dispersed trans-Golgi network mediates NLRP3 inflammasome activation, Nature, 564, 71, 10.1038/s41586-018-0761-3 Magupalli, 1979, HDAC6 mediates an aggresome-like mechanism for NLRP3 and pyrin inflammasome activation, Science, 2020, 369 He, 2016, NEK7 is an essential mediator of NLRP3 activation downstream of potassium efflux, Nature, 530, 354, 10.1038/nature16959 Sharif, 2019, Structural mechanism for NEK7-licensed activation of NLRP3 inflammasome, Nature, 570, 338, 10.1038/s41586-019-1295-z Boucher, 2018, Caspase-1 self-cleavage is an intrinsic mechanism to terminate inflammasome activity, J. Exp. Med., 215, 827, 10.1084/jem.20172222 Lu, 2014, Unified polymerization mechanism for the assembly of ASC-dependent Inflammasomes, Cell, 156, 1193, 10.1016/j.cell.2014.02.008 Magupalli, 1979, HDAC6 mediates an aggresome-like mechanism for NLRP3 and pyrin inflammasome activation, Science, 2020 Schmidt, 2016, A single domain antibody fragment that recognizes the adaptor ASC defines the role of ASC domains in inflammasome assembly, J. Exp. Med., 213, 771, 10.1084/jem.20151790 Xia, 2021, Gasdermin D pore structure reveals preferential release of mature interleukin-1, Nature, 593, 607, 10.1038/s41586-021-03478-3 Evavold, 2018, The pore-forming protein gasdermin D regulates interleukin-1 secretion from living macrophages, Immunity, 48, 35, 10.1016/j.immuni.2017.11.013 Rühl, 2018, ESCRT-dependent membrane repair negatively regulates pyroptosis downstream of GSDMD activation, Science, 362, 956, 10.1126/science.aar7607 Broz, 2020, The gasdermins, a protein family executing cell death and inflammation, Nat. Rev. Immunol., 20, 143, 10.1038/s41577-019-0228-2 Wang, 2020, Structural mechanism for GSDMD targeting by autoprocessed caspases in Pyroptosis, Cell, 180, 941, 10.1016/j.cell.2020.02.002 Aglietti, 2016, GsdmD p30 elicited by caspase-11 during pyroptosis forms pores in membranes, Proc. Natl. Acad. Sci. U. S. A., 113, 7858, 10.1073/pnas.1607769113 Kayagaki, 2021, NINJ1 mediates plasma membrane rupture during lytic cell death, Nature, 591, 131, 10.1038/s41586-021-03218-7 Torre-Minguela, 2021, Gasdermins mediate cellular release of mitochondrial DNA during pyroptosis and apoptosis, FASEB J., 35, 1, 10.1096/fj.202100085R Baroja-Mazo, 2014, The NLRP3 inflammasome is released as a particulate danger signal that amplifies the inflammatory response, Nat. Immunol., 15, 738, 10.1038/ni.2919 Franklin, 2014, The adaptor ASC has extracellular and “prionoid” activities that propagate inflammation, Nat. Immunol., 15, 727, 10.1038/ni.2913 Zanoni, 2016, An endogenous caspase-11 ligand elicits interleukin-1 release from living dendritic cells, Science (New York, N.Y.), 352, 1232, 10.1126/science.aaf3036 Kayagaki, 1979, Noncanonical inflammasome activation by intracellular LPS independent of TLR4, Science, 2013, 1246 Schmid-Burgk, 2015, Caspase-4 mediates non-canonical activation of the NLRP3 inflammasome in human myeloid cells, Eur. J. Immunol., 45, 2911, 10.1002/eji.201545523 Baker, 2015, NLRP3 inflammasome activation downstream of cytoplasmic LPS recognition by both caspase-4 and caspase-5, Eur. J. Immunol., 45, 2918, 10.1002/eji.201545655 Kayagaki, 2011, Non-canonical inflammasome activation targets caspase-11, Nature, 479, 117, 10.1038/nature10558 Kayagaki, 2015, Caspase-11 cleaves gasdermin D for non-canonical inflammasome signalling, Nature, 526, 666, 10.1038/nature15541 Deets, 2021, Inflammasomes and adaptive immune responses, Nat. Immunol., 22, 412, 10.1038/s41590-021-00869-6 Karki, 2019, Diverging inflammasome signals in tumorigenesis and potential targeting, Nat. Rev. Cancer, 19, 197, 10.1038/s41568-019-0123-y Missiroli, 2021, Targeting the NLRP3 inflammasome as a new therapeutic option for overcoming cancer, Cancers, Vol 13, 2297, 10.3390/cancers13102297 Mangan, 2018, Targeting the NLRP3 inflammasome in inflammatory diseases, Nat. Rev. Drug Discov., 17, 588, 10.1038/nrd.2018.97 Swanson, 2019, The NLRP3 inflammasome: molecular activation and regulation to therapeutics, Nat. Rev. Immunol., 19, 477, 10.1038/s41577-019-0165-0 de Torre-Minguela, 2017, Mesa del Castillo P, Pelegrín P. the NLRP3 and pyrin Inflammasomes: implications in the pathophysiology of autoinflammatory diseases. Frontiers in, Immunology, 8, 43 Tapia-Abellán, 2019, MCC950 closes the active conformation of NLRP3 to an inactive state, Nat. Chem. Biol., 15, 560, 10.1038/s41589-019-0278-6 Mensa-Vilaro, 2016, Late onset cryopyrin-associated periodic syndrome due to myeloid-restricted somatic NLRP3 mosaicism, Arthritis Rheum., 68, 3035, 10.1002/art.39770 Bertoni, 2020, A novel knock-in mouse model of cryopyrin-associated periodic syndromes with development of amyloidosis: therapeutic efficacy of proton pump inhibitors, J. Allergy Clin. Immunol., 145, 368, 10.1016/j.jaci.2019.05.034 Brydges, 2009, Inflammasome-mediated disease animal models reveal roles for innate but not adaptive immunity, Immunity, 30, 875, 10.1016/j.immuni.2009.05.005 Meng, 2009, A mutation in the Nlrp3 gene causing inflammasome hyperactivation potentiates Th17 cell-dominant immune responses, Immunity, 30, 860, 10.1016/j.immuni.2009.04.012 Klück, 2020, Dapansutrile, an oral selective NLRP3 inflammasome inhibitor, for treatment of gout flares: an open-label, dose-adaptive, proof-of-concept, phase 2a trial, Lancet Rheumatol., 2, e270, 10.1016/S2665-9913(20)30065-5 Wohlford, 2020, Phase 1B, randomized, double-blinded, dose escalation, single-center, repeat dose safety and pharmacodynamics study of the Oral NLRP3 inhibitor Dapansutrile in subjects with NYHA II-III systolic heart failure, J. Cardiovasc. Pharmacol., 77, 49, 10.1097/FJC.0000000000000931 Alarcón-Vila, 2019, Purinergic receptors and the inflammatory response mediated by lipids, Curr. Opin. Pharmacol., 47, 90, 10.1016/j.coph.2019.02.004 Wymann, 2008, Lipid signalling in disease, Nat. Rev. Mol. Cell Biol., 9, 162, 10.1038/nrm2335 Elliott, 2018, Cutting edge: mitochondrial assembly of the NLRP3 Inflammasome complex is initiated at priming, J. Immunol., 200, 3047, 10.4049/jimmunol.1701723 Ohto, 2022, Structural basis for the oligomerization-mediated regulation of NLRP3 inflammasome activation, Proc. Natl. Acad. Sci. U. S. A., 119, 10.1073/pnas.2121353119 de la Roche, 2018, Trafficking of cholesterol to the ER is required for NLRP3 inflammasome activation, J. Cell Biol., 217, 3560, 10.1083/jcb.201709057 Ruysschaert, 2015, Role of lipid microdomains in TLR-mediated signalling, Biochim. Biophys. Acta Biomembr., 1848, 1860, 10.1016/j.bbamem.2015.03.014 Angosto-Bazarra, 2021, Techniques to study Inflammasome activation and inhibition by small molecules, Molecules, 26, 1704, 10.3390/molecules26061704 Platt, 2016, Immune dysfunction in Niemann-pick disease type C, J. Neurochem., 136, 74, 10.1111/jnc.13138 Iyer, 2013, Mitochondrial cardiolipin is required for NLRP3 inflammasome activation, Immunity, 39, 311, 10.1016/j.immuni.2013.08.001 Pizzuto, 2020, Cardiolipin in immune signaling and cell death, Trends Cell Biol., 30, 892, 10.1016/j.tcb.2020.09.004 Tapia-Abellán, 2021, Sensing low intracellular potassium by NLRP3 results in a stable open structure that promotes inflammasome activation, Sci. Adv., 7, 10.1126/sciadv.abf4468 Berliner, 2009, The role of oxidized phospholipids in atherosclerosis, J. Lipid Res., 50, S207, 10.1194/jlr.R800074-JLR200 Aguilar-Ballester, 2020, Impact of cholesterol metabolism in immune cell function and atherosclerosis, Nutrients, 12, 1, 10.3390/nu12072021 Corrêa, 2020, Lysophosphatidylcholine induces NLRP3 inflammasome-mediated foam cell formation and pyroptosis in human monocytes and endothelial cells, Front. Immunol., 10, 2927, 10.3389/fimmu.2019.02927 Grebe, 2013, Cholesterol crystals and inflammation, Curr. Rheumatol. Rep., 15, 313, 10.1007/s11926-012-0313-z Duewell, 2010, NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals, Nature, 464, 1357, 10.1038/nature08938 Zanoni, 2016, An endogenous caspase-11 ligand elicits interleukin-1 release from living dendritic cells, Science, 352, 1232, 10.1126/science.aaf3036 Chu, 2018, The oxidized phospholipid oxPAPC protects from septic shock by targeting the non-canonical inflammasome in macrophages, Nat. Commun., 9, 996, 10.1038/s41467-018-03409-3 Chang, 2004, Apoptotic cells with oxidation-specific epitopes are immunogenic and proinflammatory, J. Exp. Med., 200, 1359, 10.1084/jem.20031763 Podrez, 2002, Identification of a novel family of oxidized phospholipids that serve as ligands for the macrophage scavenger receptor CD36, J. Biol. Chem., 277, 38503, 10.1074/jbc.M203318200 Watson, 1999, Structural identification of a novel pro-inflammatory epoxyisoprostane phospholipid in mildly oxidized low density lipoprotein, J. Biol. Chem., 274, 24787, 10.1074/jbc.274.35.24787 Gaidt, 2016, Human monocytes engage an alternative Inflammasome pathway, Immunity, 44, 833, 10.1016/j.immuni.2016.01.012 Yeon, 2017, Oxidized phosphatidylcholine induces the activation of NLRP3 inflammasome in macrophages, J. Leukoc. Biol., 101, 205, 10.1189/jlb.3VMA1215-579RR Oskolkova, 2010, Oxidized phospholipids are more potent antagonists of lipopolysaccharide than inducers of inflammation, J. Immunol., 185, 7706, 10.4049/jimmunol.0903594 Liu-Wu, 1998, Lysophosphatidylcholine induces the production of IL-1β by human monocytes, Atherosclerosis, 137, 351, 10.1016/S0021-9150(97)00295-5 Stock, 2006, Lysophosphatidylcholine stimulates IL-1β release from microglia via a P2X 7 receptor-independent mechanism, J. Immunol., 177, 8560, 10.4049/jimmunol.177.12.8560 Rajamäki, 2010, Cholesterol crystals activate the NLRP3 Inflammasome in human macrophages: a novel link between cholesterol metabolism and inflammation, PLoS One, 5, 10.1371/journal.pone.0011765 Cao, 2020, Multiple roles of 25-hydroxycholesterol in lipid metabolism, antivirus process, inflammatory response, and cell survival, Oxidative Med. Cell. Longev., 2020, 10.1155/2020/8893305 Jang, 2016, 25-hydroxycholesterol contributes to cerebral inflammation of X-linked adrenoleukodystrophy through activation of the NLRP3 inflammasome, Nat. Commun., 7, 10.1038/ncomms13129 Reboldi, 1979, 25-hydroxycholesterol suppresses interleukin-1-driven inflammation downstream of type I interferon, Science, 2014, 679 Alegría Ezquerra, 2008, Obesity, metabolic syndrome and diabetes: cardiovascular implications and therapy, Rev. Esp. Cardiol., 61, 752, 10.1157/13123996 Vandanmagsar, 2011, The NLRP3 inflammasome instigates obesity-induced inflammation and insulin resistance, Nat. Med., 17, 179, 10.1038/nm.2279 Luheshi, 2012, Sphingosine regulates the NLRP3-inflammasome and IL-1β release from macrophages, Eur. J. Immunol., 42, 716, 10.1002/eji.201142079 Yan, 2013, Omega-3 fatty acids prevent inflammation and metabolic disorder through inhibition of NLRP3 Inflammasome activation, Immunity, 38, 1154, 10.1016/j.immuni.2013.05.015 L’homme, 2013, Unsaturated fatty acids prevent activation of NLRP3 inflammasome in human monocytes/macrophages, J. Lipid Res., 54, 2998, 10.1194/jlr.M037861 Gianfrancesco, 2019, Saturated fatty acids induce NLRP3 activation in human macrophages through K + efflux resulting from phospholipid saturation and Na, K-ATPase disruption, Biochim. Biophys. Acta Mol. Cell Biol. Lipids, 1864, 1017, 10.1016/j.bbalip.2019.04.001 Karasawa, 2018, Saturated fatty acids undergo intracellular crystallization and activate the NLRP3 Inflammasome in macrophages, Arterioscler. Thromb. Vasc. Biol., 38, 744, 10.1161/ATVBAHA.117.310581 Wen, 2011, Fatty acid–induced NLRP3-ASC inflammasome activation interferes with insulin signaling, Nat. Immunol., 12, 408, 10.1038/ni.2022 de Carvalho, 2019, Leishmania lipophosphoglycan triggers Caspase-11 and the non-canonical activation of the NLRP3 inflammasome, Cell Rep., 26, 429, 10.1016/j.celrep.2018.12.047 Aachoui, 1979, Caspase-11 protects against bacteria that escape the vacuole, Science, 2013, 975 Santos, 2018, LPS targets host guanylate-binding proteins to the bacterial outer membrane for non-canonical inflammasome activation, EMBO J., 37, 10.15252/embj.201798089 Hagar, 1979, Cytoplasmic LPS activates Caspase-11: implications in TLR4-independent endotoxic shock, Science, 2013, 1250 Deng, 2018, The endotoxin delivery protein HMGB1 mediates Caspase-11-dependent lethality in Sepsis, Immunity, 0, 1 Santos, 2018, Sensing of invading pathogens by GBPs: at the crossroads between cell-autonomous and innate immunity, J. Leukoc. Biol., 104, 729, 10.1002/JLB.4MR0118-038R Meunier, 2014, Caspase-11 activation requires lysis of pathogen-containing vacuoles by IFN-induced GTPases, Nature, 509, 366, 10.1038/nature13157 Lagrange, 2018, Human caspase-4 detects tetra-acylated LPS and cytosolic Francisella and functions differently from murine caspase-11, Nat. Commun., 9, 10.1038/s41467-017-02682-y Gay, 2007, Structure and function of {Toll} receptors and their ligands, Annu. Rev. Biochem., 76, 141, 10.1146/annurev.biochem.76.060305.151318 Santos, 2020, Human GBP1 binds LPS to initiate assembly of a caspase-4 activating platform on cytosolic bacteria, Nat. Commun., 11, 10.1038/s41467-020-16889-z Wandel, 2020, Guanylate-binding proteins convert cytosolic bacteria into caspase-4 signaling platforms, Nat. Immunol., 21, 880, 10.1038/s41590-020-0697-2 Brubaker, 2020, A rapid Caspase-11 response induced by IFNγ priming is independent of guanylate binding proteins, IScience, 23, 10.1016/j.isci.2020.101612 Pizzuto, 2022, Ornithine lipid activates both TLR4 and the non-canonical NLRP3 Inflammasome, BioRxiv Kim, 2018, Bacterial ornithine lipid, a surrogate membrane lipid under phosphate-limiting conditions, plays important roles in bacterial persistence and interaction with host, Environ. Microbiol., 20, 3992, 10.1111/1462-2920.14430 Barbosa, 2018, Accumulation of ornithine lipids in Vibrio cholerae under phosphate deprivation is dependent on VC0489 (OlsF) and PhoBR system, Microbiol. (U. K.), 164, 395, 10.1099/mic.0.000607 Vences-Guzmán, 2012, Ornithine lipids and their structural modifications: from A to E and beyond, FEMS Microbiol. Lett., 335, 1, 10.1111/j.1574-6968.2012.02623.x Córdoba-Castro, 2021, Ornithine lipids in Burkholderia spp. Pathogenicity, Front. Mol. Biosci., 7, 457, 10.3389/fmolb.2020.610932 Okemoto, 2008, The preparation of a lipidic endotoxin affects its biological activities, Biol. Pharm. Bull., 31, 1952, 10.1248/bpb.31.1952 Kawai, 1989, Macrophage activation by an ornithine-containing lipid or a serine-containing lipid, Infect. Immun., 57, 2086, 10.1128/iai.57.7.2086-2091.1989 Kawai, 1991, Protection of mice from lethal endotoxemia by use of an ornithine-containing lipid or a serine-containing lipid, Infect. Immun., 59, 2560, 10.1128/iai.59.8.2560-2566.1991 Lonez, 2008, Cationic liposomal lipids: from gene carriers to cell signaling, Prog. Lipid Res., 47, 340, 10.1016/j.plipres.2008.03.002 Witzigmann, 2020, Lipid nanoparticle technology for therapeutic gene regulation in the liver, Adv. Drug Deliv. Rev., 159, 344, 10.1016/j.addr.2020.06.026 Felgner, 1987, Lipofection: a highly efficient, lipid-mediated {DNA}-transfection procedure, Proc. Natl. Acad. Sci. U. S. A., 84, 7413, 10.1073/pnas.84.21.7413 Akinc, 2019, The Onpattro story and the clinical translation of nanomedicines containing nucleic acid-based drugs, Nat. Nanotechnol., 14, 1084, 10.1038/s41565-019-0591-y S S, J F, H A, KI K, K H, N I, 1997, Human immunodeficiency virus type-1-specific immune responses induced by DNA vaccination are greatly enhanced by mannan-coated diC14-amidine, Eur. J. Immunol., 27, 3121, 10.1002/eji.1830271207 Jacquet, 2005, Vaccination with the recombinant allergen ProDer p 1 complexed with the cationic lipid DiC14-amidine prevents allergic responses to house dust mite, Mol. Ther., 11, 960, 10.1016/j.ymthe.2004.12.024 Wilmar, 2012, The cationic lipid, diC14 amidine, extends the adjuvant properties of aluminum salts through a TLR-4- and caspase-1-independent mechanism, Vaccine, 30, 414, 10.1016/j.vaccine.2011.10.071 Tahtinen, 2022, IL-1 and IL-1ra are key regulators of the inflammatory response to RNA vaccines, Nat. Immunol., 23, 532, 10.1038/s41590-022-01160-y Pizzuto, 2016, Toll-like receptor 2 promiscuity is responsible for the immunostimulatory activity of nucleic acid nanocarriers, J. Control. Release, 247, 182, 10.1016/j.jconrel.2016.12.029 Lonez, 2015, Critical residues involved in toll-like receptor 4 activation by cationic lipid nanocarriers are not located at the lipopolysaccharide-binding interface, Cell. Mol. Life Sci., 72, 3971, 10.1007/s00018-015-1915-1 Lonez, 2014, Cationic lipid nanocarriers activate toll-like receptor 2 and NLRP3 inflammasome pathways, Nanomedicine, 10, 775, 10.1016/j.nano.2013.12.003 Lonez, 2009, Cationic lipids activate cellular cascades. Which receptors are involved?, Biochim. Biophys. Acta Gen. Subj., 1790, 425, 10.1016/j.bbagen.2009.02.015 Pizzuto, 2018, Cationic lipids as one-component vaccine adjuvants: a promising alternative to alum, J. Control. Release, 287, 67, 10.1016/j.jconrel.2018.08.020 Qin, 1997, Promoter attenuation in gene therapy: interferon-gamma and tumor necrosis factor-alpha inhibit transgene expression, Hum. Gene Ther., 8, 2019, 10.1089/hum.1997.8.17-2019 He, 2019, Membrane fusogenic lysine type lipid assemblies possess enhanced NLRP3 inflammasome activation potency, Biochem. Biophys. Rep., 18 Li, 2018, Lysine-containing cationic liposomes activate the NLRP3 inflammasome: effect of a spacer between the head group and the hydrophobic moieties of the lipids, Nanomedicine, 14, 279, 10.1016/j.nano.2017.10.011 Samaridou, 2020, Lipid nanoparticles for nucleic acid delivery: current perspectives, Adv. Drug Deliv. Rev., 154–155, 37, 10.1016/j.addr.2020.06.002 Dinarello, 2018, Overview of the IL-1 family in innate inflammation and acquired immunity, Immunol. Rev., 281, 8, 10.1111/imr.12621 Lee, 2003, Lipid-protein interactions in biological membranes: a structural perspective, Biochim. Biophys. Acta, 1612, 1, 10.1016/S0005-2736(03)00056-7