Cited by 1,330Inflammasome and immune disordersPancreatic function and diabetesDiabetes and associated disorders

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Activation of the NLRP3 inflammasome by islet amyloid polypeptide provides a mechanism for enhanced IL-1β in type 2 diabetes

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Masters, Seth L, Dunne, Aisling, Subramanian, Shoba L, Hull, Rebecca L, Tannahill, Gillian M, Sharp, Fiona A, Becker, Christine, Franchi, Luigi, Yoshihara, Eiji, Chen, Zhe, Mullooly, Niamh, Mielke, Lisa A, Harris, James, Coll, Rebecca C, Mills, Kingston H G, Mok, K Hun, Newsholme, Philip, Nuñez, Gabriel, Yodoi, Junji, Kahn, Steven E, Lavelle, Ed C, O'Neill, Luke A J·2010·Nature Immunology

DOI 10.1038/ni.1935PMC PMC3103663

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Abstract

Interleukin 1β (IL-1β) is an important inflammatory mediator of type 2 diabetes. Here we show that oligomers of islet amyloid polypeptide (IAPP), a protein that forms amyloid deposits in the pancreas during type 2 diabetes, triggered the NLRP3 inflammasome and generated mature IL-1β. One therapy for type 2 diabetes, glyburide, suppressed IAPP-mediated IL-1β production in vitro. Processing of IL-1β initiated by IAPP first required priming, a process that involved glucose metabolism and was facilitated by minimally oxidized low-density lipoprotein. Finally, mice transgenic for human IAPP had more IL-1β in pancreatic islets, which localized together with amyloid and macrophages. Our findings identify previously unknown mechanisms in the pathogenesis of type 2 diabetes and treatment of pathology caused by IAPP.

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Fermentation Products of Paenibacillus bovis sp. nov. BD3526 Alleviates the Symptoms of Type 2 Diabetes Mellitus in GK Rats
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Emerging Biomarkers and Nanobiosensing Strategies in Diabetes
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METTL3 Modulates TXNIP Expression to Affect the Activation of NLRP3 Inflammasome in Hepatic Cells Under Oxygen–Glucose Deprivation/Reperfusion Injury
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Perceptions of the Use of Mobile Technologies for Smoking Cessation: Focus Group Study With Individuals of Low Socioeconomic Status Who Smoke
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Cutaneous manifestations of systemic autoinflammatory disorders
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Sulfonylureas for Treatment of Periodontitis-Diabetes Comorbidity-Related Complications: Killing Two Birds With One Stone
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“Glyburide is the first identified compound to prevent cryopyrin activation and microbial ligand-, DAMPs-, and crystal-induced IL-1β secretion (Lamkanfi et al., 2009; Masters et al., 2010).”
Background
Conformation-reconstructed multivalent antibody mimic for amplified mitigation of human islet amyloid polypeptide amyloidogenesis
Zhao, L., Wang, S., Hu, Q., Jia, H., Xin, Y., Luo, L., & Meng, F. (2022) · Nanoscale · doi:10.1039/d1nr08090c · Cited by 10
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Mechanisms of ag85a/b DNA vaccine conferred immunotherapy and recovery from Mycobacterium tuberculosis ‐induced injury
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“The expressions of genes IAPP, Slc30a8, Scg2, Chga, and Chgb were significantly reduced, which can protect islet B cells from apoptosis and can also change the insulin secretion defect caused by the inflammatory environment of pancreatic islets, thus improving the function of islet B cells and reducing the risk of TB…”
BackgroundInfluential
SAA1 exacerbates pancreatic β-cell dysfunction through activation of NF-κB signaling in high-fat diet-induced type 2 diabetes mice
Wang, Q., Li, H., Lu, H., Wang, S., Li, Y., Zhang, Z., Han, J., Yang, Z., Yang, Y., & Hong, Y. (2023) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2023.112043 · Cited by 10
Role of β‐cell autophagy in β‐cell physiology and the development of diabetes
Yasasilka, X. R., & Lee, M. (2024) · Journal of Diabetes Investigation · doi:10.1111/jdi.14184 · Cited by 12
“The mechanism of b -cell death by hIAPP oligomer is unclear, although ER stress 38 , ER translocon clogging 39 , in ﬂ ammasome activation 40 or membrane pore formation 41,42 have been implicated.”
Background
NLRP3 Inflammasome Sequential Changes in Staphylococcus aureus-Induced Mouse Model of Acute Rhinosinusitis
Wang, Y., Gong, G.-Q., Chen, S., Xiong, L.-Y., Zhou, X., Huang, X., & Kong, W.-J. (2014) · International Journal of Molecular Sciences · doi:10.3390/ijms150915806 · Cited by 10
“We presumed that the NLRP3 inflammasome was activated resulting in an inflammatory cascade after inoculation, and then some endogenous NLRP3 agonists, for example, adenosine triphosphate and glucose, were released and activated more NLRP3 inflammasomes [19,21].”
Background
The Role of Interleukin-1β in Destruction of Transplanted Islets
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Non-classical circulating monocytes in severe obesity and obesity with uncontrolled diabetes: A comparison with tuberculosis and healthy individuals
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Anti-inflammatory properties of antidiabetic agents
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Regulating against the dysregulation: new treatment options in autoinflammation
Kallinich, T. (2015) · Seminars in Immunopathology · doi:10.1007/s00281-015-0501-9 · Cited by 10
The Emerging Roles of IL-36, IL-37, and IL-38 in Diabetes Mellitus and its Complications
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Long noncoding RNA maternally expressed gene 3 improves trophoblast dysfunction and inflammation in preeclampsia through the Wnt/β-Catenin/nod-like receptor pyrin domain-containing 3 axis
Yue, L., Wang, P., Shi, Y., Cui, B., & Meng, J. (2022) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2022.1022450 · Cited by 9
“The nod-like receptor pyrin domaincontaining 3 (NLRP3) inflammasome is an oligomeric complex that has been confirmed to be closely linked to many inflammatory and autoimmune diseases, such as atherosclerosis, gout, and diabetes mellitus (Masters et al., 2010; Davis et al., 2011; Karasawa and Takahashi, 2017; So and Ma…”
Background
IAPP - oligomerisation levels in plasma of people with type 2 diabetes
Rehn, F., Kraemer‐Schulien, V., Bujnicki, T., Bannach, O., Tschoepe, D., Stratmann, B., & Willbold, D. (2024) · Scientific Reports · doi:10.1038/s41598-024-70255-3 · Cited by 10
“Furthermore, IAPP is a potent activator of the NLRP3 inflammasome, leading to the production of the proinflammatory cytokine IL-1β, which is known to promote insulin resistance and ultimately damage β-cells in the long term 18 .”
Greasing the wheels of inflammasome formation: regulation of NLRP3 function by S-linked fatty acids
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Targeting the NLRP3 inflammasome in Parkinson's disease: From molecular mechanism to therapeutic strategy
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Inflammasomes: novel therapeutic targets for metabolic syndrome?
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Vegan and Plant-Based Diets in the Management of Metabolic Syndrome: A Narrative Review from Anti-Inflammatory and Antithrombotic Perspectives
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Post-translational modifications of NLRP3: to prime or not to prime?
Dufies, O., & Zanoni, I. (2025) · Trends in Immunology · doi:10.1016/j.it.2025.10.008 · Cited by 11
The role of pancreatic islet macrophages in type 2 diabetes mellitus: from underlying pathological mechanisms to therapeutic target discovery
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“This drives the transcription of pro-inflammatory cytokines such as TNF-α and IL-6, and facilitating NLRP3 inflammasome assembly [70].”
Native and oxidised lipoproteins negatively regulate the serum amyloid A‐induced NLRP3 inflammasome activation in human macrophages
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Immune cell infiltration in the pancreas of type 1, type 2 and type 3c diabetes
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Association of inflammatory cytokines with obesity and pulmonary function testing
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Characteristics of elderly diabetes patients: focus on clinical manifestation, pathogenic mechanism, and the role of traditional Chinese medicine
Yang, X., Xue, C., Chen, K.-Y., Gao, D., Wang, H., & Tang, C. (2024) · Frontiers in Pharmacology · doi:10.3389/fphar.2023.1339744 · Cited by 6
RETRACTED: Monocytes play different roles in stimulating T cells in obese diabetic individuals
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Retracted
Measuring IL-1β Processing by Bioluminescence Sensors II: The iGLuc System
Bartok, E., Kampes, M., & Hornung, V. (2016) · Methods in molecular biology · doi:10.1007/978-1-4939-3566-6_6 · Cited by 9
Genetic disruption of the inflammasome adaptor ASC has minimal impact on the pathogenesis of Duchenne muscular dystrophy in mdx Mice
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Targeting SARS‐CoV‐2 RBD Interface: a Supervised Computational Data‐Driven Approach to Identify Potential Modulators
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Inflammasomes: Role in Disease Pathogenesis and Therapeutic Potential
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KN3014, a piperidine-containing small compound, inhibits auto-secretion of IL-1β from PBMCs in a patient with Muckle–Wells syndrome
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Polyphenolic Gallotannins 1,3,6-Tri-O-galloyl-β- d -glucose and Corilagin Attenuate IAPP Amyloid Formation and Cytotoxicity by Primarily Targeting Secondary Nucleation
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Pancreatic Islet Cell Hormones: Secretion, Function, and Diabetes Therapy
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“Similarly, islet amyloid polypeptide (IAPP), a proteinresponsibleforamyloiddepositioninthepancreasinT2D, activates the NLRP3 inflammasome and produces mature IL-1 β [203].”

Authors: Masters, S. L., Dunne, A., Subramanian, S. L., Hull, R. L., Tannahill, G. M., Sharp, F. A., Becker, C., Franchi, L., Yoshihara, E., Chen, Z., Mullooly, N., Mielke, L. A., Harris, J., Coll, R. C., Mills, K. H. G., Mok, K. H., Newsholme, P., Nuñez, G., Yodoi, J., Kahn, S. E., Lavelle, E. C., & O'Neill, L. A. J.
Affiliations: Trinity College Dublin (IE)
University of Washington (US)
University of Michigan (US)
Kyoto University (JP)
University College Dublin (IE)
Corresponding author: Masters, Seth L
ORCID: Masters, Seth L
Dunne, Aisling
Subramanian, Shoba L
Hull, Rebecca L
Becker, Christine
Yoshihara, Eiji
Chen, Zhe
Mielke, Lisa A
Harris, James
Coll, Rebecca C
Mills, Kingston H G
Mok, K Hun
Newsholme, Philip
Kahn, Steven E
Lavelle, Ed C
O'Neill, Luke A J
Venue: Nature Immunology
Publisher: Springer Science and Business Media LLC
Published: 2010-09-12
Volume: 11
Issue: 10
Pages: 897-904
ISSN: 1529-2908 (ISSN-L)
1529-2916
DOI: 10.1038/ni.1935
PMC: PMC3103663
OpenAlex: W2034946303
Cited by: 1,330
References: 55
Citations by year: 2026: 58 · 2025: 57 · 2024: 64 · 2023: 75 · 2022: 71 · 2021: 99 · 2020: 100 · 2019: 95 · 2018: 82 · 2017: 83 · 2016: 73 · 2015: 101 · 2014: 95 · 2013: 112 · 2012: 83
FWCI: 35.67
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
Locations: Nature Immunology (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
HAL (submittedVersion, other-oa)
eSpace (Curtin University) (submittedVersion)
Trinity's Access to Research Output (TARA) (Trinity College Dublin) (submittedVersion)
Funders: National Institute of Allergy and Infectious Diseases (AI063331, R56AI063331, R01AI063331, R37AI063331)
National Institute of Diabetes and Digestive and Kidney Diseases (DK-75998, R01DK075998)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Inflammasome and immune disorders
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Pancreatic function and diabetes
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Diabetes and associated disorders
Keywords: NLRP3 inflammasome, amylin, IL-1β, type 2 diabetes, beta cell destruction, glibenclamide, LDL oxidation, glucose metabolism, inflammasome priming, pancreatic islets, macrophages, amyloid deposition
MeSH terms: NLR Family, Pyrin Domain-Containing 3 Protein, Amyloid, Animals, Carrier Proteins, Cells, Cultured, Dendritic Cells, Diabetes Mellitus, Type 2, Glyburide, Humans, Hypoglycemic Agents, Islets of Langerhans, Macrophages, Mice, Inbred C57BL, Mice, Transgenic, Receptors, Cytoplasmic and Nuclear, Mice, Rats, Interleukin-1beta, Islet Amyloid Polypeptide

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Activation of the NLRP3 inflammasome by islet amyloid polypeptide provides a mechanism for enhanced IL-1β in type 2 diabetes

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