Cited by 790Inflammasome and immune disordersImmune Response and InflammationAutoimmune and Inflammatory Disorders Research

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The NLRP3 inflammasome is released as a particulate danger signal that amplifies the inflammatory response

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Baroja-Mazo, Alberto, Martín-Sánchez, Fatima, Gomez, Ana I, Martínez, Carlos M, Amores-Iniesta, Joaquín, Compan, Vincent, Barberà-Cremades, Maria, Yagüe, Jordi, Ruiz-Ortiz, Estibaliz, Antón, Jordi, Buján, Segundo, Couillin, Isabelle, Brough, David, Arostegui, Juan I, Pelegrín, Pablo·2014·Nature Immunology

DOI 10.1038/ni.2919

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Abstract

Assembly of the NLRP3 inflammasome activates caspase-1 and mediates the processing and release of the leaderless cytokine IL-1β and thereby serves a central role in the inflammatory response and in diverse human diseases. Here we found that upon activation of caspase-1, oligomeric NLRP3 inflammasome particles were released from macrophages. Recombinant oligomeric protein particles composed of the adaptor ASC or the p.D303N mutant form of NLRP3 associated with cryopyrin-associated periodic syndromes (CAPS) stimulated further activation of caspase-1 extracellularly, as well as intracellularly after phagocytosis by surrounding macrophages. We found oligomeric ASC particles in the serum of patients with active CAPS but not in that of patients with other inherited autoinflammatory diseases. Our findings support a model whereby the NLRP3 inflammasome, acting as an extracellular oligomeric complex, amplifies the inflammatory response.

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Background
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Background
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Background
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Result
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Influential
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Background
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Background
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Background
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Background
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Pioglitazone ameliorates retinal ischemia/reperfusion injury via suppressing NLRP3 inflammasome activities
Zhang, Y.-L., Wang, R.-B., Li, W.-Y., Xia, F., & Liu, L. (2017) · International Journal of Ophthalmology · doi:10.18240/ijo.2017.12.04 · Cited by 22
The mechanism of NLRP3 inflammasome initiation: Trimerization but not dimerization of the NLRP3 pyrin domain induces robust activation of IL-1β
Sušjan, P., Roškar, S., & Hafner‐Bratkovič, I. (2017) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2017.01.008 · Cited by 22
NOD-like receptors in fish: evolution, structure, immune signaling, and targeting for aquaculture vaccine adjuvants
Swain, B., & Miryala, K. R. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1665071 · Cited by 23
Biological mechanisms of non-linear dose-response for respirable mineral fibers
Cox, L. A. (2018) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2018.06.016 · Cited by 21
Novel presentations of periodic fever syndromes: Discrepancies between genetic and clinical diagnoses
Hoang, T. K., & Albert, D. (2018) · European Journal of Rheumatology · doi:10.5152/eurjrheum.2018.18023 · Cited by 21
“The NALP3 inflammasome is also activated by macrophages which increases the inflammation (8, 9).”
Background
Zebrafish Models to Study Inflammasome-Mediated Regulation of Hematopoiesis
Rodríguez‐Ruiz, L., Lozano‐Gil, J. M., Lachaud, C., Mesa-del-Castillo, P., Cayuela, M. L., García‐Moreno, D., Pérez‐Oliva, A. B., & Mulero, V. (2020) · Trends in Immunology · doi:10.1016/j.it.2020.10.006 · Cited by 20
Imaging Approaches to Monitor Inflammasome Activation
Nandi, D., Farid, N. S. S., Karuppiah, H. A. R., & Kulkarni, A. A. (2021) · Journal of Molecular Biology · doi:10.1016/j.jmb.2021.167251 · Cited by 20
Spatiotemporal evolution of pyroptosis and canonical inflammasome pathway in hSOD1G93A ALS mouse model
Zhang, H., Li, H., Huang, B., Wang, S., Gao, Y., Meng, F., Chen, Y., Zhou, F., Guan, Y., & Wang, X. (2022) · BMC Neuroscience · doi:10.1186/s12868-022-00733-9 · Cited by 22
“in the spinal cord of ALS mice NLRP3 is crucial for subsequent activation of the other inflammasome components [13].”
Background
Orally Delivered Connexin43 Hemichannel Blocker, Tonabersat, Inhibits Vascular Breakdown and Inflammasome Activation in a Mouse Model of Diabetic Retinopathy
Mugisho, O. O., Aryal, J., Shome, A., Lyon, H., Acosta, M. L., Green, C. R., & Rupenthal, I. D. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24043876 · Cited by 21
Dose-response modeling of NLRP3 inflammasome-mediated diseases: asbestos, lung cancer, and malignant mesothelioma as examples
Cox, L. A. (2019) · Critical Reviews in Toxicology · doi:10.1080/10408444.2019.1692779 · Cited by 21
Mislocalization of the interferon inducible protein IFI16 by environmental insults: Implications in autoimmunity
Bawadekar, M., Andrea, M. D., Gariglio, M., & Landolfo, S. (2014) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2014.10.003 · Cited by 23
“[59] shows that upon inflammasome activation, functional oligomeric inflammasome particles consisting of NLRP3 and ASC are released in the extracellular environment.”
Background
The Relationship of Sphingosine Kinase 1 With Pyroptosis Provides a New Strategy for Tumor Therapy
Wang, X., Yang, Y., Cai, W.-Q., & Lü, Y. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.574990 · Cited by 20
An Atypical Autoinflammatory Disease Due to an LRR Domain NLRP3 Mutation Enhancing Binding to NEK7
Caseley, E. A., Reyna, S. J. L., Poulter, J. A., Topping, J., Carter, C. R. D., Nadat, F., Spickett, G. P., Savic, S., & McDermott, M. (2021) · Journal of Clinical Immunology · doi:10.1007/s10875-021-01161-w · Cited by 20
AllergoOncology: Danger signals in allergology and oncology: A European Academy of Allergy and Clinical Immunology (EAACI) Position Paper
Bergmann, C., Poli, A., Agache, I. O., Bianchini, R., Bax, H. J., Castells, M., Crescioli, S., Dombrowicz, D., Ferastraoaru, D. E., Fiebiger, E., et al. (2022) · Allergy · doi:10.1111/all.15255 · Cited by 20
Alcohol-induced extracellular ASC specks perpetuate liver inflammation and damage in alcohol-associated hepatitis even after alcohol cessation
Ribeiro, M. D. C., Iracheta‐Vellve, A., Babuta, M., Calenda, C. D., Copeland, C., Zhuang, Y., Lowe, P., Hawryluk, D., Catalano, D., Cho, Y., et al. (2023) · Hepatology · doi:10.1097/hep.0000000000000298 · Cited by 21
“Several reports have described the in vitro role of macrophages in ASC specks release upon LPS plus nigericin treatment.[8,9] While we focused on macrophages and hepatocytes in this study, we cannot rule out the participation of other cells, such as neutrophils, which have been shown to induce inflammasome activation…”
BackgroundInfluential
Role of NLRP3 Inflammasome in Stroke Pathobiology: Current Therapeutic Avenues and Future Perspective
Panbhare, K., Pandey, R., Chauhan, C., Sinha, A., Shukla, R., & Kaundal, R. K. (2023) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.3c00536 · Cited by 21
Mechanistic insights into the oncolytic activity of vesicular stomatitis virus in cancer immunotherapy
Wan, Y., Simovic, B., & Walsh, S. R. (2015) · Oncolytic Virotherapy · doi:10.2147/ov.s66079 · Cited by 20
Downregulation of signal transduction and STAT3 expression exacerbates oxidative stress mediated by NLRP3 inflammasome
Bai, H., Zhang, Q., Duan, J., Yu, D., & Liu, L. (2018) · Neural Regeneration Research · doi:10.4103/1673-5374.241470 · Cited by 20
“Nucleotide binding to the oligonucleotide receptor protein 3 (NLRP3) inflammasomes are important players in inflammation and are associated with neurodegenerative diseases (Baroja-Mazo et al., 2014).”
Background
Risk Analysis Implications of Dose-Response Thresholds for NLRP3 Inflammasome-Mediated Diseases: Respirable Crystalline Silica and Lung Cancer as an Example
Cox, L. A. (2019) · Dose-Response · doi:10.1177/1559325819836900 · Cited by 20
An innate interaction between IL-18 and the propeptide that inactivates its precursor form
Tsutsumi, N., Ayumi, Y., Kimura, T., Kato, Z., Fukao, T., Shirakawa, M., Ohnishi, H., & Tochio, H. (2019) · Scientific Reports · doi:10.1038/s41598-019-42661-5 · Cited by 18
Alendronate augments lipid A-induced IL-1β release and Smad3/NLRP3/ASC-dependent cell death
Tamai, R., & Kiyoura, Y. (2018) · Life Sciences · doi:10.1016/j.lfs.2018.02.014 · Cited by 21
Signalling by co-operative higher-order assembly formation: linking evidence at molecular and cellular levels
Kobe, B., Nanson, J. D., Hoad, M., Blumenthal, A., Gambin, Y., Sierecki, E., Stacey, K. J., Ve, T., & Halfmann, R. (2025) · Biochemical Journal · doi:10.1042/bcj20220094 · Cited by 25
“Beyond being restricted to individual cells, there is some evidence for signal transduction between cells [145,146]; how common this is, remains an open question.”
Techniques to Study Inflammasome Activation and Inhibition by Small Molecules
Angosto-Bazarra, D., Molina‐López, C., Peñín‐Franch, A., Hurtado‐Navarro, L., & Pelegrín, P. (2021) · Molecules · doi:10.3390/molecules26061704 · Cited by 19
“Alternatives to measure release of IL-1β or IL-18 are to measure other proteins such as ASC, high motility group box 1 (HMGB1), or inflammasome sensors that can be released during pyroptosis upon inflammasome activation [78].”
Background
Aberrant NLRP3 Inflammasome Activation Ignites the Fire of Inflammation in Neuromuscular Diseases
Péladeau, C. L., & Sandhu, J. K. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22116068 · Cited by 20
Chicken macrophages infected with Salmonella (S.) Enteritidis or S. Heidelberg produce differential responses in immune and metabolic signaling pathways
He, H., Arsenault, R. J., Genovese, K. J., Johnson, C. N., & Kogut, M. H. (2017) · Veterinary Immunology and Immunopathology · doi:10.1016/j.vetimm.2017.11.002 · Cited by 19
The burden of subclinical intra‐articular inflammation in gout
Chowalloor, P., Raymond, W. D., Cheah, P., & Keen, H. I. (2020) · International Journal of Rheumatic Diseases · doi:10.1111/1756-185x.13811 · Cited by 19
“Number of joints with PD ≥ 2 5 (3-9) 0-17 3 (0-4) 0-6 .”
Differential Effect of Extracellular Acidic Environment on IL-1β Released from Human and Mouse Phagocytes
Sušjan, P., Benčina, M., & Hafner‐Bratkovič, I. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21197229 · Cited by 20
“Immunofluorescent labeling of endogenous ASC was performed in fixed and permeabilized WT iBMDMs, as previously described [45,47].”
Method
Clustering of NLRP3 induced by membrane or protein scaffolds promotes inflammasome assembly
Boršić, E., Ramuta, T. Ž., Orehek, S., Kreft, M. E., Geyer, M., Jerala, R., & Hafner‐Bratkovič, I. (2025) · Nature Communications · doi:10.1038/s41467-025-60277-4 · Cited by 21
Extracellular NLRP3 inflammasome particles are internalized by human coronary artery smooth muscle cells and induce pro-atherogenic effects
Gaul, S., Schaeffer, K. M., Opitz, L., Maeder, C., Kögel, A., Uhlmann, L., Kalwa, H., Wagner, U. G., Haas, J., Behzadi, A., et al. (2021) · Scientific Reports · doi:10.1038/s41598-021-94314-1 · Cited by 20
Inflammasome Meets Centrosome: Understanding the Emerging Role of Centrosome in Controlling Inflammasome Activation
Wu, D., Zhang, Z., Jiang, X., Du, Y., Zhang, S., & Yang, X. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.826106 · Cited by 20
“Not only that, the NLRP3 inflammasome speck can be even released to extracellular space where it is still functioning to amplify inflammatory responses (44).”
Background
Emerging Concepts in Innate Immunity
Pelka, K., & Nardo, D. D. (2017) · Methods in molecular biology · doi:10.1007/978-1-4939-7519-8_1 · Cited by 19
A Paradox in Bacterial Pathogenesis: Activation of the Local Macrophage Inflammasome Is Required for Virulence of Streptococcus uberis
Archer, N., Egan, S. A., Coffey, T. J., Emes, R. D., Addis, M. F., Ward, P. N., Blanchard, A. M., & Leigh, J. A. (2020) · Pathogens · doi:10.3390/pathogens9120997 · Cited by 18
“uberis is likely mediated by Caspase 1, as Ac-YVAD-cmk is a highly selective inhibitor of caspase 1, with some activity against caspase 4 [54,55], (although its activity against the bovine-specific caspase 13—an orthologue of caspase 4—is unknown).”
Background
Ameliorative Effects of Cardamonin on Monosodium Urate-Induced Gouty Arthritis through Inhibiting NLRP3 Inflammasome Mediation
Wang, C.-C., Lu, J.-W., Peng, Y.-J., Lee, C. H., Lee, H.-S., Chu, Y.-H., Huang, C.-J., Ho, Y.-J., Liu, F.-C., & Wu, C.-C. (2021) · Medicina · doi:10.3390/medicina57090898 · Cited by 17
“Some evidence also shows that caspase-1 activates pro-IL-1β as well as pro-interleukin-18 (pro-IL-18) and converts them into active IL-1β and interleukin-18 (IL-18), respectively [12,13].”
Background
Nano-Selenium Modulates NF-κB/NLRP3 Pathway and Mitochondrial Dynamics to Attenuate Microplastic-Induced Liver Injury
Shen, Q., Liu, Y., Li, J., & Zhou, D. (2024) · Nutrients · doi:10.3390/nu16223878 · Cited by 17
Syphilitic infection impairs immunity by inducing both apoptosis and pyroptosis of CD4 + and CD8 + T lymphocytes
Xia, W., Zhao, J., Su, B., Jiao, Y., Weng, W., Zhang, M., Wang, X., Guo, C., Wu, H., Zhang, T., et al. (2020) · Innate Immunity · doi:10.1177/1753425920952840 · Cited by 16
“These processes are in marked contrast to the packaging of cellular contents and non-inflammatory phagocytic uptake of membrane-bound apoptotic bodies that characterize apoptosis.(19,20) In contrast to pyroptosis, apoptosis, another kind of programmed cell death mainly mediated by the effector caspase-3, is a fundamen…”
Background
NLRP3 inflammasome activation and symptom burden in KRAS-mutated CMML patients is reverted by IL-1 blocking therapy
Hurtado‐Navarro, L., Cuenca‐Zamora, E. J., Zamora, L., Bellosillo, B., Such, E., Soler‐Espejo, E., Martínez‐Banaclocha, H., Hernández‐Rivas, J. M., Marco, J., Martínez-Alarcón, L., et al. (2023) · Cell Reports Medicine · doi:10.1016/j.xcrm.2023.101329 · Cited by 17
Tryptanthrin suppresses multiple inflammasome activation to regulate NASH progression by targeting ASC protein
Ren, L., Yang, H., Wang, H., Qin, S., Zhan, X., Li, H., Wei, Z., Fang, Z., Li, Q., Liu, T., et al. (2024) · Phytomedicine · doi:10.1016/j.phymed.2024.155758 · Cited by 18
A novel selective NLRP3 inhibitor shows disease-modifying potential in animal models of Parkinson’s disease
Chatterjee, A., Mohapatra, J., Sharma, M., Jha, A., Patro, R., Das, D., Patel, H., Patel, H., Chaudhari, J., Borda, N., et al. (2024) · Brain Research · doi:10.1016/j.brainres.2024.149129 · Cited by 17
Activation of the Innate Immune Receptors: Guardians of the Micro Galaxy
Nardo, D. D. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-981-10-5987-2_1 · Cited by 16
The neutrophil inflammasome
Tyrkalska, S. D., Candel, S., & Mulero, V. (2020) · Developmental & Comparative Immunology · doi:10.1016/j.dci.2020.103874 · Cited by 18

Authors: Baroja-Mazo, A., Martín-Sánchez, F., Gomez, A. I., Martínez, C. M., Amores-Iniesta, J., Compan, V., Barberà-Cremades, M., Yagüe, J., Ruiz-Ortiz, E., Antón, J., Buján, S., Couillin, I., Brough, D., Arostegui, J. I., & Pelegrín, P.
Affiliations: Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (ES)
University of Manchester (GB)
Hospital Clínic de Barcelona (ES)
Hospital Sant Joan de Déu Barcelona (ES)
Vall d'Hebron Hospital Universitari (ES)
Université d'Orléans (FR)
ORCID: Martínez, Carlos M
Compan, Vincent
Yagüe, Jordi
Antón, Jordi
Couillin, Isabelle
Brough, David
Pelegrín, Pablo
Venue: Nature Immunology
Publisher: Springer Science and Business Media LLC
Published: 2014-06-22
Volume: 15
Issue: 8
Pages: 738-748
ISSN: 1529-2908 (ISSN-L)
1529-2916
DOI: 10.1038/ni.2919
OpenAlex: W2143119237
Cited by: 790
References: 50
Citations by year: 2026: 28 · 2025: 39 · 2024: 41 · 2023: 63 · 2022: 81 · 2021: 84 · 2020: 86 · 2019: 68 · 2018: 74 · 2017: 88 · 2016: 60 · 2015: 57 · 2014: 20
FWCI: 30.77
Type: journal article
Language: en
Open access: green
hdl.handle.net
Licence: cc-by-nc-nd
www.springer.com/tdm (tdm)
Locations: Nature Immunology (publishedVersion)
PubMed (publishedVersion)
Hispana (publishedVersion, cc-by-nc-nd)
Research Explorer (The University of Manchester) (submittedVersion)
Funders: Wellcome Trust
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Inflammasome and immune disorders
Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
Health Sciences › Medicine › Hematology › Autoimmune and Inflammatory Disorders Research
Keywords: NLRP3 inflammasome, caspase-1, IL-1β processing, cryopyrin-associated periodic syndromes, macrophages, autoinflammatory disease, phagocytosis
MeSH terms: NLR Family, Pyrin Domain-Containing 3 Protein, Animals, Carrier Proteins, Cells, Cultured, Cytoskeletal Proteins, Humans, Inflammation, Macrophages, Mice, Inbred C57BL, Phagocytosis, Signal Transduction, Mice, Knockout, Caspases, Caspase 1, Apoptosis Regulatory Proteins, Mice, CARD Signaling Adaptor Proteins, Caspases, Initiator, Interleukin-1beta, Cryopyrin-Associated Periodic Syndromes, HEK293 Cells, Inflammasomes

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The NLRP3 inflammasome is released as a particulate danger signal that amplifies the inflammatory response

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